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Master recyclers: features and
functions of bacteria associated with
phytoplankton blooms
Alison Buchan1, Gary R. LeCleir1, Christopher A. Gulvik2 and José M. González3
Abstract | Marine phytoplankton blooms are annual spring events that sustain active and
diverse bloom-associated bacterial populations. Blooms vary considerably in terms of
eukaryotic species composition and environmental conditions, but a limited number of
heterotrophic bacterial lineages — primarily members of the Flavobacteriia, Alphaproteo-
bacteria and Gammaproteobacteria — dominate these communities. In this Review, we
discuss the central role that these bacteria have in transforming phytoplankton-derived
organic matter and thus in biogeochemical nutrient cycling. On the basis of selected field
and laboratory-based studies of flavobacteria and roseobacters, distinct metabolic strategies
are emerging for these archetypal phytoplankton-associated taxa, which provide insights
into the underlying mechanisms that dictate their behaviours during blooms.
Phytoplankton, such as diatoms and coccolithophores, in a patchy distribution of bacterial activity throughout
Autotrophs
Organisms that convert are free-floating photosynthetic organisms that are the oceans6. Copiotrophic bacteria, which swiftly capital-
inorganic carbon, such as CO, found in aquatic environments. These organisms capture ize on increased carbon and nutrient concentrations at
2
into organic compounds. energy from sunlight and transform inorganic matter both the microscale and macroscale, complement their
into organic matter (which is known as biomass). In the oligotrophic counterparts, which prefer dilute nutrient
Biological pump
ocean, this organic matter is the foundation of a com- concentrations. Together, the heterotrophic bacteria,
The export of phytosynthetically
derived carbon via the sinking plex marine food web, which relies heavily on microbial which use these two distinct trophic strategies balance
of particles from the illuminated transformation: approximately one-half of the carbon marine productivity.
surface ocean to the deep that is fixed by marine autotrophs is directly processed by Microbially transformed carbon has several possible
ocean. Approximately 0.1% of
bacteria1,2. The remaining carbon either enters the classic fates in the ocean (FIG. 1); for example, microbial respira-
the carbon that is fixed in the
ocean is buried in marine marine food web or is transported as sinking particles tion converts carbon to an inorganic, gaseous state as
sediments via this process. to the deep ocean for long-term storage via the biological CO that is released into the atmosphere. Phytoplankton-
2
pump3 (FIG. 1). Localized and transient increases in the derived carbon can also enter the microbial loop, where it
abundance of phytoplankton are referred to as blooms is first converted into microbial biomass and can either
1Department of Microbiology, and result in a boost in biogeochemical activities, includ- be transferred up the food web as bacteria succumb to
University of Tennessee, ing the assimilation of CO and inorganic nutrients, predation by organisms at higher trophic levels (such
Knoxville, Tennessee 2
such as nitrogen and phosphorus4,5. These processes are as zooplankton) or remain in the microbial domain
37996-0845, USA.
2School of Civil and partly balanced by a subsequent increase in the activity of via continual recycling7. Alternatively, a fraction of the
Environmental Engineering, heterotrophi c bacteria, which transform phytoplankton- microbially transformed carbon is released into the dis-
Georgia Institute of derived organic matter. As phytoplankton blooms are solved phase, some of which resists degradation and
Technology, Atlanta,
often seasonal in nature and are thus transient events, contributes to the large pool of recalcitrant dissolved
Georgia 30332, USA.
the abundance and activity of heterotrophic bacteria organic carbon (DOC) that is stored in the ocean for
3Department of Microbiology,
University of La Laguna, varies accordingly. Indeed, secondary bacterial pro- thousands of years via the microbial carbon pump8. In
ES-38200 La Laguna, Spain. duction typically correlates with the concentration addition, bacteria also regenerate nutrients that are
Correspondence to A.B. of chlorophyll a, which is a proxy for phytoplankton associated with phytoplankton organic matter, particu-
e-mail: [email protected]
abundance2. This correlation between primary and larly nitrogen and phosphorus7. Although it is not dis-
doi:10.1038/nrmicro3326
Published online secondary production is evident on both small (that is, cussed in depth here, viral lysis of heterotrophic bacteria
19 August 2014 micromolar) and large (that is, basin) scales and results and phytoplankton is an important mechanism for the
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CO Bacteria–phytoplankton interactions during bloom
2
events are complex and change throughout the lifetime
of the bloom. Bacteria can support the growth of phyto-
CO
2 CO2 plankton via the recycling of nutrients, but at the same
time, they also compete with phytoplankton for essen-
tial nutrients. Both healthy and dead (or dying) phyto-
1 Phytoplankton Zooplankton plankton release organic compounds that are consumed
3
by heterotrophic bacteria, and the chemical nature and
concentration of the released compounds varies with
phytoplankton species and the physiological status of
the phytoplankton10,11. Phytoplankton species show vari-
2 ation in their biochemical composition and the relative
DOM POM cellular proportions of proteins, fatty acids, sugars and
nucleic acids12–14. This variation in composition influ-
DOC, DON and DOP POC, PON and POP
ences both the stoichiometry, such as the C/N/P ratio,
4
and bioreactivity of phytoplankton-derived POM and
Microbial loop
DOM, which in turn influences the metabolic activity
and proliferation of heterotrophic bacteria and dictates
Heterotrophic their growth efficiencies as well as the fate of microbially
P bacteria
transformed organic matter6.
P
N P Despite the variation in phytoplankton composition
N
N and environmental conditions, a limited number of taxa
Inorganic
are consistently found to dominate bloom-associated
nutrients
Biological bacterial communities. The most frequent bacteria that
6
pump are identified by 16S ribosomal RNA gene-based sur-
Microbial
carbon pump 5 veys are members of the classes Flavobacteriia (hereafter
7 Viral shunt
referred to as flavobacteria), Alphaproteobacteria, includ-
ing members of the Rhodobacteraceae (such as roseo-
bacters), and Gammaproteobacteria, such as members
Long-term storage
of the Alteromonadaceae15–17. The metabolic properties
Figure 1 | Bacterial transformation of phytoplankton-derived organic matter. The of these bacteria enable their ready response to transient
Nature Reviews | Microbiology
marine carbon cycle includes a number of processes, several of which are mediated by nutrient pulses, which are a hallmark of phytoplankton
microorganisms. Key processes of the marine carbon cycle include the conversion of blooms. Moreover, several laboratory studies have iden-
inorganic carbon (such as CO) to organic carbon by photosynthetic phytoplankton tified specific associations between phytoplankton and
2
species (step 1); the release of both dissolved organic matter (DOM; which includes certain species of roseobacters and flavobacteria. As such,
dissolved organic carbon (DOC), dissolved organic nitrogen (DON) and dissolved organic
these two bacterial groups have emerged as the main
phosphorous (DOP)) and particulate organic matter (POM; which includes particulate
models for the study of microorganism–phytoplankton
organic carbon (POC), particulate organic nitrogen (PON) and particulate organic
interactions.
phosphorous (POP)) from phytoplankton (step 2); the consumption of phytoplankton
This Review provides a brief overview of marine
biomass by zooplankton grazers (step 3) and the mineralization (that is the release of CO
via respiration during the catabolism of organic matter) and recycling of organic matter 2 phytoplankton blooms and highlights recent advances
by diverse heterotrophic bacteria, including, but not limited to, flavobacteria and in our understanding of the composition, dynamics and
roseobacters (which is known as the microbial loop; step 4). A fraction of the physiologies of bloom-associated bacteria. Owing to the
heterotrophic bacteria is consumed by zooplankton, and the carbon is further variation in the types of naturally occurring blooms, it
transferred up the food web. Heterotrophic bacteria also contribute to the is difficult to depict a generalized bloom scenario that
remineralization of organic nutrients, including DON and DOP, to inorganic forms, adequately encompasses the complexity of all of the
which are then available for use by phytoplankton. The microbial carbon pump (step 5)
observed systems. Instead, the objective here is to pro-
refers to the transformation of organic carbon into recalcitrant DOC that resists further
vide an overview of the most common bloom events and
degradation and is sequestered in the ocean for thousands of years. The biological pump
describe our understanding of microbial–phytoplankto n
(step 6) refers to the export of phytoplankton-derived POM from the surface oceans to
interactions for flavobacteria and roseobacters, which
deeper depths via sinking. Finally, the viral shunt (step 7) describes the contributions of
viral-mediated cell lysis to the release of dissolved and particulate matter from both the are the two most well-described bacterial lineages
phytoplankton and bacterial pools. (BOX 1). Data from both laboratory and field-based stud-
ies provide a framework for developing a mechanistic
understanding of the factors that drive bacterial com-
release of both dissolved organic matter (DOM) and par- munity composition and activity during phytoplankton
ticulate organic matter (POM) into the ocean. This viral blooms. Our ability to understand the roles that indi-
Heterotrophic
A term used to describe an ‘shunt’ redirects carbon and nutrients away from higher vidual bacterial species have in both the formation of
organism that uses organic trophic levels and towards the microbial realm9 (FIG. 1). blooms and their eventual collapse, will ultimately lead
carbon compounds, such as Various biological and environmental factors determine to a better understanding of the forces that control
dissolved organic matter and
how photosynthetically fixed carbon is processed by het- energy flow in the ocean as well as the cycling of com-
particulate organic matter, to
satisfy its carbon requirement erotrophic bacteria in the ocean, and thereby determine pounds that influence climate change, including CO2
but that cannot fix carbon. its allocation among these reservoirs. and organosulphur compounds.
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although blooms are typically classified according to
Box 1 | Defining the Roseobacter and Flavobacteria lineages
a dominant species that persists for the lifetime of the
Although the use of the terms Roseobacter and Flavobacteria to describe bloom (BOX 2). Compared with natural blooms, experi-
phylogenetically cohesive groups of marine bacteria is common in the microbial ecology
mental phytoplankton blooms, which are generated
literature, their use can be confusing as they do not conform to the Linnaean classification
by the controlled use of defined nutrients, usually
system. Members of the Roseobacter clade belong to the Rhodobacteraceae family in
develop and collapse within 1 or 2 weeks27. During both
the Alphaproteobacteria class of the Proteobacteria. The group name derives from the
natural and experimental blooms, there is a high diver-
genus of the first two described strains (Roseobacter denitrificans and Roseobacter
litoralis), but the clade currently contains many more than the 50 described genera and sity of associated organisms that includes not only a
thousands of uncharacterized species and strains. With few exceptions, all of the succession of phytoplankton but also a clear progression
identified strains and 16S ribosomal RNA gene sequences that belong to this family are of protistan grazers, bacteria and viruses26,28–31. Bloom
derived from marine or saline environments15. The polyphyletic nature of the decline may occur in response to ‘top-down’ forces (such
Rhodobacteriaceae 16S rRNA gene makes phylogenetic reconstructions of the lineage as grazing and viral lysis), ‘bottom-up’ forces (such as
challenging74 and hinders the development of nucleic acid-based molecular tools that nutrient limitation) or a combination of both24,29,32,33.
are both specific and inclusive125. It could be argued that the borders that define the
The organic matter that is released by a declining bloom
Roseobacter lineage are diffuse. Roseobacters were mostly ignored by microbiologists
provides a wide range of nutritional resources, many of
and ecologist until the early 1990s, when culture-independent approaches to assess
which can be exploited by the associated heterotrophic
microbial diversity were applied to marine systems and led to the recognition of this
bacterial community. During bloom collapse, organic
group as one of the most abundant bacterial groups in the oceans68.
Flavobacteria is a term that is used to describe bacteria that belong to the molecules from dying phytoplankton frequently aggre-
Flavobacteriia class in the Bacteroidetes phylum. Efforts have been made to decipher gate to form composites of detrital particles, which are
the taxonomy of this phylum in recent decades, but the results have sometimes been readily colonized by heterotrophic bacteria34. Particle
controversial126. This class currently contains a single order, the Flavobacteriales, and aggregation is mediated by large, sticky and acidic poly-
four families (Flavobacteriaceae, Blattabacteriaceae, Cryomorphaceae and saccharides, which are collectively known as transpar-
Schleiferiaceae), two of which (that is, Flavobacteriaceae and Cryomorphaceae) ent exopolymer particles (TEPs). TEPs can lead to the
contain marine representatives. Most Blattabacteriaceae are obligate symbionts and
formation of sinking detrital particles that transport
the Schleiferiaceae family consists of a single genus (that is, Schleiferia). By contrast,
phytoplankton material from surface waters to the
Flavobacteriaceae is an extraordinarily diverse family that contains more than 100
deep ocean35.
genera, whereas the Cryomorphaceae family includes novel psychrotolerant genera
Molecules that are produced by phytoplankton can
(that is, genera that are tolerant to low temperatures)127. Both culture-dependent and
-independent methods have determined the ubiquity of flavobacteria representatives also influence the climate on both local and global
in diverse habitats, including the mammalian digestive tract, soil and aquatic scales. In addition to their involvement in aggregation
environments113. Representative strains of flavobacteria have been readily isolated and transport, TEPs can be encapsulated and released
from marine environments since at least the mid-1950s128 and are found in various to the lower atmosphere via sea surface spray. Further-
niches, but they are usually most abundant in coastal waters and in phytoplankton more, some phytoplankton produce large amounts
blooms104. However, group members are frequently underrepresented in 16S rRNA of the organic sulphur compound dimethylsulphonio-
gene surveys as a result of technical difficulties — that is, standard primers for the 16S
pro pionate (DMSP) during bloom events, which, as
rRNA gene function poorly in flavobacteria104. Given the prevalence and culturability
discussed below, can be converted to the gas dimethyl
of both marine roseobacters and flavobacteria there has been increased interest in
sulphide (DMS) via various biochemical pathways, some
elucidating their metabolic potential and activities in the past 2 decades. Many of
of which are encoded by algae and some of which are
these investigations are facilitated by the availability of dozens of genome sequences
for isolated representatives or single cell amplified genomes (SAGs)77,110. encoded by members of the bacterial community36. DMS
emissions from surface seawaters are the major source of
sulphur in the atmosphere37. Together with other marine
Common features of phytoplankton blooms aerosols, both TEPs and DMS influence the regional and
Most phytoplankton blooms develop in the spring global climate by functioning as cloud condensation nuclei
months in response to higher intensity (or longer dura- and affecting solar backscattered radiation37,38.
tion) of light exposure, combined with higher sea sur-
face temperatures, reduced grazing pressure and higher Bacterial responses to phytoplankton blooms
nutrient levels owing to seasonal mixing events18–20. Measurements of bulk community parameters have
Depending on the biological, chemical and physical shown that phytoplankton blooms provide an environ-
factors that control a given system, blooms can range ment that increases the rate of bacterial growth and
from localized to massively scaled events (>100,000 km2 production30,39,40. The abundance of bacterial cells is
Copiotrophic
(FIG. 2)). Nitrogen, phosphorus, iron and silicate are generally positively correlated with the abundance of
A term used to describe an
organism that thrives in, and is among the most common nutrients that influence both phytoplankton during the bloom (FIG. 2c). However, there
well adapted to, high-nutrient the initiation and termination of a bloom, and the bal- is often an initial decoupling of bacterial and phyto-
conditions, unlike oligotrophic ance of these elements often drives the establishment plankton populations at the earliest stage of a bloom;
organisms, which are adapted of specific phytoplankton species21–24. However, it is for example, an abrupt initial decrease in the abundance
to growth in low-nutrient
not yet clear if there is a single, globally dominant factor of bacterioplankton, followed by a subsequent increase, is
conditions.
that triggers the many spring phytoplankton blooms that frequently, but not always17, observed30 (FIG. 2c). The cause
Microbial loop occur annually worldwide, and this remains an area of of the initial decline in bacterial abundance is not fully
The microbial assimilation of active research and debate25. understood, but it might result from bacterial predation
dissolved organic matter into
Natural phytoplankton blooms typically last from by protists41 or from competition with phytoplankton
biomass and its transfer to
higher trophic levels as a result weeks to months and are characterized by a succession for nutrients28. Irrespective of the cause, the bacterial
of grazing by zooplankton. of several different phytoplankton species17,26 (FIG. 2), population rapidly recovers after the initial decrease
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a
and becomes abundant, as organic matter is released by
the large phytoplankton population at the height of the
bloom and during its decline. Indeed, the levels of bac-
teria remain high immediately following the collapse of
a bloom, as bacteria continue to use the organic matter
that is released from dying phytoplankton42.
Changes in the abundance and types of phytoplank-
A ton species, coupled with bacterial degradation of POM
Microbial carbon pump 50 km and DOM, alters both the concentration and composi-
tion of the detrital pools at different times during the
A process by which a major
reservoir of dissolved organic b bloom, which, in turn, drives the composition and
carbon is sequestered in the activity of the associated bacterial communities. In the
ocean by a series of earliest stages of a bloom, phytoplankton release solu-
heterotrophic microbial
ble, labile, low molecular weight (LMW) molecules,
transformations of organic
matter, which renders it such as amino acids, organic acids, carbohydrates and
increasingly resistant to sugar alcohols10,43,44, which might function as chemo-
biological degradation. B attractants for beneficial bacteria45, including bacteria
that produce phytoplankton growth-promoting com-
Dissolved organic matter
pounds, such as vitamins. The release of small molecules
(DOM). The pool of organic
matter that is operationally 50 km by living phytoplankton often increases in response to
defined as that which passes nutrient-limiting conditions, which occur at the height
through a filter with pores of of the bloom, and further stimulates heterotrophic bac-
0.22–0.45 µm in diameter. c
Bloom onset Bloom collapse terial activity46,47. During the waning stages of the bloom,
DOM can be further classified
on the basis of bioavailability. phytoplankton release higher molecular weight macro-
e molecules (HMW), including polysaccharides, proteins,
Particulate organic matter nc nucleic acids and lipids, as well as particulate material,
a
(POM). The pool of organic nd primarily as result of cell lysis6,11,48, although several
matter that is operationally u
defined as that which is e ab HMW compounds are also released from viable cells35,
roef t0a.in2e2d– 0on.4 a5 f µiltmer i nw ditiha mpoerteesr . elativ pbaecrthearpiasl tcoo msumstuaninit ym. utualistic interactions with the
R
Cloud condensation nuclei
Bacterial conversion of organic matter. Bloom-associate d
Aerosols (that is, liquid droplets
or solid particles) suspended in heterotrophic bacteria are fuelled by the assimilation
the air that lead to the Time (weeks) and remineralization of phytoplankton organic matter.
condensation of water vapour Owing to the heterogeneous chemical nature of this
to form clouds. Bacteria Nanoflagellates Picophytoplankton organic matter, the processes involved are complex
Diatoms Dinoflagellates
and are not yet fully understood49,50. An initial step
Solar backscattered
radiation Figure 2 | A representative bloom in the southern in the transformation of the bioavailable particulate
Nature Reviews | Microbiology
Solar radiation from the sun Pacific Ocean. Spring phytoplankton blooms are a fraction of organic matter is its conversion to the dis-
that is reflected back towards natural part of the seasonal productivity cycle of many solved phase (that is, DOM), which enables transport
space by the atmosphere,
marine systems. These blooms are transient events that across the bacterial cell wall. This conversion is influ-
clouds and the surface of the
Earth. typically last for several weeks and are large enough to enced by many factors, but the main requirement is the
be visible from space. a | A satellite image of the eastern availability and action of extracellular and cell surface-
Bacterioplankton coast of New Zealand before a bloom on 11 October associated enzymes6. Indeed, shifts in substrate-uptake
Free-living, planktonic bacteria 2009 is shown. b | The satellite image shows the same capabilities31, increases in extracellular and cell surface-
and archaea that reside in an region during a diatom-dominated bloom on 29 October
associated hydrolytic enzyme activities17,30 and changes
aquatic system. 2009. Such blooms are annual occurrences in this region
in the hydrophilic and hydrophobic properties of the
and the phytoplankton composition of these blooms
Linnaean classification have been characterized26. c | The graph shows a typical bacterial cell surface51 have been documented in bloom-
system succession of phytoplankton groups during the course associated bacteria. Furthermore, senescent phyto-
The taxonomic nomenclature
of a spring phytoplankton bloom in this region of the plankton cells and aggregates are rapidly colonized by
that was developed by Carl
Linnaeus, in which distinct ocean, which often lasts for many weeks (data taken bacteria that have a full range of hydrolytic enzymes
hierarchical groups, such as from REF. 26). Changes in the relative abundance of for efficient particle solubilization, and high extracel-
phylum, class, order, family, heterotrophic bacteria and nanoflagellate grazers are lular enzyme activities have been reported for bacteria
genus and species are defined. also indicated to show the increase in bacterial that are attached to senescent diatom cells34. After this
abundance in response to increases in phytoplankton,
initial conversion of POM, DOM is rapidly assimilated
Remineralization in addition to the increase in grazers in response to
The transformation of organic increases in their prey populations (such as bacteria and into microbial biomass and a fraction of the carbon is
matter to an inorganic form. respired as CO.
phytoplankton). The satellite images were captured by 2
This term is most often used to the Moderate Resolution Imaging Spectroradiometer It should be noted that not all phytoplankton-
describe the conversion of
(MODIS) on NASA Aqua satellite during the 2009 austral derived organic matter is susceptible to microbial
organic carbon to CO, which is
a central component o2f the spring and were generated by R. Simmon and J. Allen, attack: a substantial fraction (~30%) of the DOM that is
carbon cycle. Ocean Colour Team, NASA, USA. released from phytoplankton is recalcitrant to microbial
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Box 2 | The dominant marine phytoplankton that are associated with blooms
The biogeochemical impact of phytoplankton blooms is strongly influenced by the dominant bloom-forming species.
Some of the major groups of blooming, unicellular marine phytoplankton are the diatoms, coccolithophores and
Phaeocystis spp. (see the figure).
Diatoms
Diatom-dominated blooms are common in coastal oceans and upwelling zones, in which nutrient levels are high in the
euphotic zone129. Indeed, diatoms are often the major photoautotroph of spring phytoplankton blooms in temperate
coastal oceans and freshwater environments130 (see the figure, part a). Diatoms are responsible for nearly one-quarter of
the global primary production131 and 40% of marine primary production, which involves the synthesis of organic
compounds from CO (REF. 132). Thus, these blooms affect benthic zone and pelagic zone food webs and are crucial for
2
sustaining fish populations in temperate seas129. Compared with other phytoplankton, diatoms tend to be highly
competitive under the environmental conditions that are characteristic of spring, such as high nutrient concentrations,
cooler temperatures and substantial variations in light exposure. Silicate is required for the synthesis of their outer cell
wall (known as a frustule)133, which is exclusive to diatoms, and structural variations between species yield a range of
unique skeletons. Following diatom cell death and decomposition, the frustules sink and accumulate in marine sediments,
producing diatomite, which is an important component of fossils and also has a commercial application as diatomaceous
earth130. It has been suggested that silicate depletion is a primary factor that determines the decline of diatom blooms24.
Part a of the figure shows the diatom Thalassiosira pseudonana134.
Coccolithophores
Coccolithophorids, specifically Emiliania huxleyi, are marine microalgae that form extensive, seasonal blooms and that have
cell densities typically in the range of 10,000 cells per ml of water21. Similarly to diatoms, coccolithophores also have a
distinct outer layer, known as the coccolith, which is composed of calcium carbonate (CaCO) and is also an important
3
component of the fossil record135. The sinking of CaCO-rich coccolithophorids and their burial in marine sediments leads to
3
loss of CO from the upper water layer; thus, they represent an important mechanism for CO sequestration. This export of
2 2
organic matter and CaCO from surface waters is a vital component of the oceanic biological pump, which transports carbon
3
to the depths of the ocean136 (FIG. 1). Coccolithophore blooms are major sinks of CO in the global oceans137, and these
2
organisms also produce the organic sulphur compound dimethylsulphoniopropionate (DMSP), which is both an important
source of sulphur to the atmosphere and an important source of carbon and reduced sulphur for some heterotrophic marine
bacteria. Coccolithophores are uncommon in freshwater systems owing to low calcium concentrations138. The main
coccolithophore in the oceans is E. huxleyi139,140 (see the figure, part b). This species can form massive blooms, particularly
in phosphorous-limited conditions22. Such blooms are often visible from space owing to the reflective nature of
coccoliths137, and several studies have suggested that E. huxleyi viruses have a role in bloom termination141.
Phaeocystis spp.
Phaeocystis spp. is another common bloom-forming phytoplankton that produces DMSP23. A characteristic property of
this genus is its ability to grow as a floating colony that comprises several hundred cells embedded in a polysaccharide gel
Euphotic zone
matrix142, which can compromise water quality143. Some of the largest Phaeocystis spp. blooms occur in polar and subpolar
The layer of the water column
regions144, where they might avoid grazing by zooplankton via the production of transparent exopolymer particles (TEPs)
that receives sufficient light to
support photosynthesis. This and/or growth in either the colonial form or as single cells145. It is estimated that members of this genus are responsible for
zone is usually the upper 200 ~10% of the annual global primary productivity23. Part c of the figure shows the prymnesiophyte Phaeocystis globosa146.
metres, but the lower Part a of the figure is reproduced, with permission, from REF. 134, © 2008 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
boundary varies as the Part b of the figure is reproduced, with permission, from REF. 140 ©2012. American Geophysical Union. All Rights
concentration of living and Reserved. Part c of the figure reprinted from J. Sea Res., 76, Rousseau, V. et al., Characterization of Phaeocystis globosa
non-living particles change the (Prymnesiophyceae), the blooming species in the Southern North Sea, 105–113, © (2013), with permission from Elsevier.
turbidity of the water.
a b c
Benthic zone
The region of the water column
that extends from immediately
above the sediment surface to
immediately below the
sediment surface. Sinking
material, such as marine snow,
accumulates in this zone.
1 μm 5 μm 1 μm
Pelagic zone
The upper region of the water
Nature Reviews | Microbiology
column that is distant from
land and from the seafloor. degradation8. Furthermore, microbial transformation of centuries to millennia)53. Thus, some metabolically
Water turbidity and light
organic matter results in a range of metabolic products transformed products of phytoplankton organic mat-
intensity do not shift the
that are remarkably different from the original material. ter can be resistant to further bacterial transformation
demarcation of the pelagic
zone. For example, the preferential use of the nitrogen compo- and can thus contribute to both short-term and long-term
nent of both DOM and POM by natural heterotrophic carbon storage in the oceans8,54.
Diatomaceous earth bacterial populations is common52, and this leads to an
The remaining particulate
increased C/N ratio in increasingly processed organic Bacterioplankton community structures. Changes in the
matter from dead and decayed
diatoms, which are heavily matter, which is characteristic of recalcitrant material abundance and species composition of phytoplankton
enriched in silica frustules. (that is, material that resists microbial degradation for during blooms leads to corresponding changes in the
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bacterial community17,30,55 (FIG. 3a). The temporal scale success of individual taxa. Owing to the substantial
of these shifts is often determined by factors that initiate physiological and genomic information that is available
the bloom, such as the type and concentration of nutri- for roseobacter and flavobacteria strains, the study of
ents, as well as temperature. As naturally occurring phy- these bacteria can complement and enable the interpreta-
toplankton blooms are generally more gradual in their tion of functional community analysis data17. As the same
development and demise than experimental blooms, the level of detail is unavailable for the Gammaproteobacteria,
shifts in bacterial community structure typically occur this class is not discussed.
over a longer timescale. As different phytoplankton spe- Analysis of bacterial populations using higher phylo-
cies release different forms of organic matter and as het- genetic resolution (that is, at the species and subspecies
erotrophic bacteria differ in their capacity to consume levels) reveals that closely related roseobacter and flavo-
and remineralize various substrates56–58, it is predicted bacteria phylotypes frequently show considerably differ-
that bacterial community structure is strongly influ- ent responses during bloom progression. For example,
enced by the composition of the phytoplankton species, during a North Sea diatom bloom succession, three dif-
and this is supported by studies of several blooms55,59,60. ferent phylotypes of flavobacteria (that is, Ulvibacter-,
By contrast, a recent study in the South Pacific ocean Polaribacter- and Formosa-related) and two roseobacter
found that two distinct bloom events, in which differ- phylotypes (that is, DC5-80-3 and NAC11-7) showed
ent proportions of diatoms and cyanobacteria were contrasting abundance patterns throughout the bloom17
observed, shared highly similar bacterial communities61. (FIG. 3b). This suggests that there is a high degree of niche
Phylogenetic analyses of bacterioplankton have been specialization among these closely related taxa. Although
carried out on both experimental and natural blooms, we currently know little about the role of individual bac-
and the higher-order taxonomic classifications of the terial phylotypes during these dynamic events, genome
most abundant bloom bacteria are now well defined. and culture-based studies of representative roseobacter
However, such studies often differ with respect to bloom and flavobacteria strains are providing valuable insights
location, duration and intensity of sampling, phyto- into the nature of potential interactions.
plankton species succession, geochemistry and tem-
perature, which prevents quantitative generalizations Physiologies of bloom-associated bacteria
of bacterial composition and responses. Nevertheless, Unlike many of the other major marine bacterial line-
a few bacterial lineages within the Proteobacteria and ages, such as the SAR86 and SAR116 clades, which are
Bacteroidetes are typically abundant in blooms, irre- either difficult to culture or have not yet been brought
spective of the dominant phytoplankton species55,62,63. into culture, there are cultivated representatives available
More detailed bacterial responses to bloom conditions, for flavobacteria and roseobacter68. Indeed, cultivated
which involve comprehensive time-series analyses of representatives from these two groups are frequently
both environmental and biological factors before, dur- isolated from blooms and in vitro enrichment cultures
ing and after a bloom have recently been reported17,61. of different phytoplankton60,69,70, and they have even been
As discussed below, these studies have shown that the found to directly attach to phytoplankton cells during
relative abundance of the different bacterial phyla and a bloom71. The activities of these bacteria can be either
subphyla vary during the time course of a single bloom, supportive of or inhibitory to phytoplankton growth,
as well as between different blooms. By contrast, the few and this seems to vary according to the age of the bloom
studies that have examined archaeal abundance and and local environmental conditions72. These findings
diversity show that the abundance of these organisms suggest that there is an intimate and dynamic rela-
decreases during blooms, which suggests that they are tionship between specific bacterial strains and their
outcompeted by bacteria and phytoplankton for nutri- phytoplankton hosts, which probably has ancient ori-
ent resources under bloom conditions64. Although phage gins, given that bacteria and eukaryotic phytoplankton
abundance can be estimated from microscopy, relatively have coexisted in the oceans for more than 200 million
little is known about the specific roles that phages have years73,74. In fact, the nature of these bacterial–phyto-
in controlling bacterial composition and abundance65, plankton interactions ranges from mutualistic to para-
but this is an emerging area of interest. sitic. Some bacteria provide their hosts with essential
Roseobacters, flavobacteria and members of the vitamins and nutrients and provide protection against
Gammaproteobacteria are typically the most dominant toxic metabolic by-products, whereas others compete
bacteria in blooms, and the abundance of these groups with their hosts for nutrients or produce algicidal com-
(which is determined by 16S rRNA gene surveys) often pounds. Several examples of the interactions between
correlates with the succession patterns of phytoplank- diatoms and their associated bacteria are available in a
ton populations30,55,62. Functional community analysis recent and comprehensive review75. In the following sec-
approaches have recently been used, including metagen- tions, we mainly discuss the physiological processes that
omic, metatranscriptomic and metaproteomic studies, are involved in the bacterial transformation of phyto-
and these have provided a more holistic view of bacte- plankton-derived organic matter, particularly those that
Phylotypes rial activities17,66,67. Despite their value, these studies often occur in the context of a bloom.
Sequences or groups of consider only higher-order taxonomic groups, and as
sequences that share a certain
such, much of the biodiversity is masked. Furthermore, Roseobacters. Given both the abundance of roseobac-
level of homology, which
enables evolutionary these types of studies reveal little about the potential ters in marine systems and the availability of cultured
relatedness to be inferred. physiological or mechanistic factors that lead to the representatives, this group has been the focus of many
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a
14 4.0 ecological, genomic and physiological studies. In this
section, we discuss the features of this group that are
3.5 predicted to be important and relevant to phytoplankton
12
blooms, but it should be noted that not all observations
3.0 Ba have been confirmed within the context of phytoplankton
3m) 10 cte blooms.
mg per 8 2.5 rial abu keyM bieomgeboecrsh eomf tihcea lR porsoecoebssaecst,e irn lcinluedaigneg a craer ibnovno,l vneidtr oin-
Chlorophyll a ( 64 21..05 ×ndance 10 pe6 gowgoeefti hntnwhe,o h rppm ihhacehyobsts u oap(nrph~edlo a4aenr.nx5ukpt sMt e omacnbnta1e)d5r d,7 ia6sn .ntu oeRdl polb ihhseneui eiogrmabh tgapereacrostn r egsttrehaf oinnasrettom lfacaoartorete nis iogn thneetanesov,rtg ea7sr7 cel aatvtpirheoghraneainrs-l
1.0 r m cally limited to the nutrient-poor open ocean (such as
l
2 Prochlorococcu s spp. and Pelagibacter spp.)78,79, which
0.5
might be key to the ecological success of this group.
Although an analysis of the collective genetic comple-
0 0
1 48 55 62 69 76 83 90 ment of roseobacters shows that the group encodes sev-
Day eral biogeochemically relevant pathways, only a subset
b 3.9 9.4 6.5 29.8 9.2 54.5 10.533.0 7.7 41.9 20.741.9 6.3 29.2 6.3 18.3 of these pathways are present in any single genome77.
Roseobacter Indeed, it is becoming clear that a specific set of genes
Other or metabolic capabilities is not representative of the
Roseobacter AS-21 lineage as a whole. Furthermore, genome analysis of
uncultivated phylotypes suggests that at least some mem-
Roseobacter OCT
bers have relatively small genomes (such as phylo type
Roseobacter NAC11-7
%) HTCC2255, which has a 2.2 Mb genome80) and differ
s ( Roseobacter DC5-80-3
d in terms of functional attributes, compared with a col-
a
a re lection of cultivated strains81. These most recent find-
eri Flavobacteria ings suggest that the ecological r-strategist model, which
act Other is often used to describe roseobacters, may not be as
b
vo NS9 broadly applicable to the group as previously suggested
a
fl Winogradskyella and highlight that niche adaptation (including whether
d
an Ulvibacter a bacterium is typically phytoplankton-associated or
cter Tenacibaculum free-living) drives the variation in both genome size and
ba Sufflavibacter content among lineage members74.
o
se Polaribacter The idea that Roseobacter lineages form intimate
o
R NS5 marine group relationships with both macroalgal and microalgal cells
NS4 marine group predates the implementation of culture-independent
studies of environmental bacteria82 and is mostly sug-
NS3a marine group
gestive of mutualistic, and potentially obligate, interac-
Formosa
tions60,83–85. However, recent studies suggest that some
Flaviramulus
specific interactions have tipped the balance from mutu-
Cryomorphaceae
alistic to pathogenic, owing to the production of algicidal
1 48 55 62 69 76 83 90
Day compounds72,86, which may be important during the
terminal stages of the bloom, when nutrient resources
Figure 3 | Changes in the abundance of roseobacter and flavobacteria phylotypes
Nature Reviews | Microbiology become limiting. As a result, phytoplankton are pos-
during a diatom-dominated bloom. A high-resolution analysis of the bacterial
sibly more susceptible to such compounds. Indeed,
community during a natural spring diatom-dominated phytoplankton bloom in the
North Sea shows the succession of specific roseobacter and flavobacteria phylotypes. a recent study suggests that a mutualistic relationship
a | Chlorophyll a measurements are a proxy for phytoplankton abundance during the can easily become pathogenic, depending on specific
course of the 90 day survey. Despite the coarse temporal resolution, it is evident that the environmental or biological cues, including the onset
increase in bacterial abundance coincides with the decline in phytoplankton (following of senescence in a phytoplankton culture72. Symbioses
an initial surge), which is probably due to the increased availability of phytoplankton between roseobacter s and specific phytoplankton are
organic matter fuelling bacterial growth. b | Compared with all other bacteria, the probably facilitated by several common characteristics
relative abundance of roseobacters and flavobacteria increased during the bloom. The
(FIG. 4), including chemotaxis towards compounds that
values above each stacked column represent the percent abundance of each group
are released by phytoplankton (for example, DMSP and
member relative to total bacteria, as determined by 16S ribosomal RNA gene sequence
amino acids)45, as well as the uptake and use of various
analysis. The relative abundances of roseobacters and flavobacteria, as well as specific
phytoplankton-derived compounds, such as DOM,
phylotypes (as indicated in the key), are dynamic throughout the bloom. These complex
dynamics are probably the result of tight coupling between these heterotrophic bacteria which are sources of carbon, sulphur, nitrogen and/or
and changing local environmental conditions, which are expected to be primarily phosphorus (for example, DMSP, urea, polyamines, tau-
mediated by alterations in the availability of phytoplankton-derived organic matter and rine, glycine betaine, methylated amines, phosphoesters
possibly inorganic nutrient levels. Data taken from REF. 17. and phosphonates)77,87–89. Genomic approaches have
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identified transporters, including those of the TRAP
(tripartite ATP-independent periplasmic), MFS (major
facilitator superfamily) and ABC (ATP-binding cassette)
families, which are probably specific for these substrates
DMS and are abundant in the genomes of roseobacters77,87.
The production of secondary metabolites is often
the basis of chemical signalling, defence and host–
microorganis m interactions90, and many roseobacters
produce a range of bioactive compounds, including sig-
nalling molecules and antimicrobial compounds (FIG. 4).
Phytoplankton The production of these two types of molecules is often
linked91–93 and may facilitate intimate interactions with
algal hosts. Several roseobacters produce quorum sens-
DMSP ing molecules, particularly N-acyl-homoserine lactones
DOM (AHLs). So far, the AHLs that have been characterized
Receptors from roseobacter isolates have some of the longest rec-
ognized acyl side chains (that is, C–C )94. In addition,
8 18
Flagellar DMS + acrylate MeSH novel quorum sensing compounds have been identi-
motor fied, including p-coumaroyl-homoserine lactone, the
Chemotaxis
proteins Adhesive production of which requires an exogenous supply
H+ structure of the aromatic compound p-coumaric acid95, which
ABC-type might be released by decaying phytoplankton72. Anti-
transporters
DMT transporter microbial molecules, including tropodithietic acid and
ADP ATP indigoidine, have been identified, and studies that are
ATP
Secondary hv synthase aimed at linking the production of these secondary
transporter H+ POM metabolites to bacterial fitness are underway93,96. The
H+/Na+
Bacteriochlorophyll a production of growth-promoting compounds, includ-
Antimicrobials ing auxins and vitamins, by roseobacters has been
proposed to facilitate mutualism with phytoplank-
AHLs ton70,72,77,87, and transport proteins that belong to the
Vitamins drug–metabolite (DMT) superfamily are anticipated
to be involved in the export of such compounds87.
Surface-associated structures, including those that
resemble holdfasts, are also common among character-
Figure 4 | Physiological features of roseobacters that facilitate associations with
ized roseobacter isolates, are important in attachment
phytoplankton. Roseobacters have many metabolic feaNtuarteusr teh Raet vpireowbsa b| Mlyi fcarcoibliitoaltoeg y
to organic particles97 and may facilitate attachment to
interactions with phytoplankton and phytodetrital material. The organic sulphur
the surfaces of living phytoplankton cells. Indeed, the
compound dimethylsulphoniopropionate (DMSP) is produced by phytoplankton and
transformed via one of two pathways: cleavage to form dimethyl sulphide (DMS) roseobacter isolate Ruegeria sp. TM1040 was found to
and acrylate or demethylation to form methanethiol (MeSH). DMS is volatile and form biofilms on the Pfiesteria-like dinoflagellate in
fluxes to the atmosphere, where it contributes to cloud formation, whereas the acrylate culture98. Finally, aerobic anoxygenic phototrophy (AAP)
by-product can be used as a carbon source by the bacteria. MeSH is also a valuable is evident in many isolated strains as well as envi-
carbon substrate, from which reduced sulphur is derived. Indeed, roseobacters use a ronmental genomes. This type of photoheterotrophic
wide range of low molecular weight, phytoplankton-derived compounds as sources of strategy requires the capture of energy from sunlight
carbon, nitrogen and phosphorus (depicted as dissolved organic matter (DOM)).
by photopigments (such as bacteriochlorophyll a and
Chemotaxis towards several of these phytoplankton-derived compounds has been
carotenoids) and the translocation of protons across the
demonstrated and roseobacters encode several transport systems that are predicted to
membrane, which produces a membrane electrochemi-
mediate the uptake of small molecules, including ATP-dependent transporters (such as
cal gradient that can be used for the production of ATP
ATP-binding cassette (ABC) transporters) and secondary transporters that may use
electrochemical gradients to mediate membrane translocation, such as TRAP (tripartite (via ATP synthases), active transport (by secondary
ATP-independent periplasmic) and drug–metabolite (DMT) type systems. TRAP transport via TRAP and DMT-type transporters) and
transporters are thought to import carboxylic acids, whereas DMT transporters are motility70,82 (FIG. 4). As discussed below, light-driven ion
thought to export secondary metabolites, including phytoplankton growth-promoting pumps are also common in flavobacteria, but the con-
compounds (such as auxins and vitamins) and antimicrobial compounds that may tribution of these photoproteins to bacterial activities
provide roseobacters with a competitive advantage when colonizing the surfaces of in the ocean is not yet understood.
phytoplankton. Quorum sensing signalling molecules, typically N-acyl homoserine
An excellent example of the tight coupling between
lactones (AHLs), are produced by many roseobacter strains and have been shown to
roseobacters and phytoplankton comes from the study
regulate the production of antimicrobial compounds in a cell density-dependent
of a single algal osmolyte, DMSP. DMSP accounts for up
manner. In addition to the oxidation of organic matter, many roseobacter genomes
to 10% of the carbon that is fixed by marine phytoplank-
encode bacteriochlorophyll a-based light-driven proton pumps that contribute to
membrane electrochemical gradients, which can be used to generate ATP via ATP ton in the sunlit layers of the ocean99, and it is produced
synthases, facilitate transport or drive flagellar motors. Adhesive structures for by several species of phytoplankton, by macroalgae and
attachment to surfaces are also commonly observed in roseobacter isolates. POM, by some aquatic vascular plants36. Concentrations of
particulate organic matter. DMSP inside dinoflagellates and prymnesiophytes, such
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as Emiliania huxleyi and Phaeocystis spp., can reach the dominant phytoplankton species, geochemical condi-
molar range99. During the demise of phytoplankton cells, tions and geographic location17,64,114, have been carried
particulate-bound DMSP is transferred to the dissolved out so far, common functional patterns are evident,
phase via grazing, autolysis and viral lysis100. The dis- particularly for flavobacteria. Metaproteomic profiling
solved DMSP is readily available for bacterial degrada- of both North Sea and Southern Ocean phytoplankton
tion, and it functions as a valuable carbon and sulphur blooms have shown that TonB-dependent transporter
source for those cells that have the proteins and enzymes (TBDT) systems that are representative of those found
that are needed for its uptake and degradation. In fact, in flavobacterial isolates are abundant during the peak
DMSP-degrading marine bacteria can satisfy nearly all of blooms17,64. Typically, TBDT systems contain outer
of their sulphur demand by DMSP consumption alone101. membrane substrate-binding proteins and cell sur-
Although sulphur concentrations are not limiting in sea- face-associated degradative enzymes (such as glycosyl
water, the reduced form that is present in DMSP is more hydrolases), which collectively facilitate the use of HMW
energetically useful to marine bacteria than the oxidized macromolecules that are present in DOM115 (FIG. 5). This
form that is found in seawater sulphate. Many culti- is in contrast to LMW transport systems, such as the
vated Roseobacter lineages are capable of transforming ABC-type and secondary transporters (that are spe-
DMSP, either by cleavage (to form DMS and acrylate) cific for free amino acids, sugars and monocarboxylic
Ecological r‑strategist model or by demethylation (to form methanethiol (MeSH))36. or dicarboxylic acids), which are frequently mapped to
Model organisms with DMS is volatile and readily escapes into the atmosphere, roseobacters during blooms17,114. In fact, the number of
relatively large genomes that
where it is proposed to contribute to the formation of transporters that are encoded in marine flavobacteria
encode diverse metabolic
capabilities, which enable them cloud condensation nuclei and to the backscatter of solar genomes is remarkably low compared with most other
to rapidly respond to increases radiation37. MeSH is more likely to remain in the sur- copiotrophic marine bacteria, including roseobac-
in carbon and nutrients. face ocean, where it is readily used by marine bacteria ters108,113,116. Carbohydrate-active enzymes that degrade
(FIG. 4). Thus, the DMSP cleavage pathway has important algal polysaccharides (such as laminarinases, which
Phytodetrital material
Non-living organic matter that implications for global climate regulation, whereas the degrade laminarin, and β-D-fucosidases, which degrade
is derived from phytoplankton. DMSP demethylation pathway is important for supply- fucose) have been found to coincide with the peak abun-
ing carbon and sulphur to marine food webs. Roseo- dances of flavobacteria17,64. Finally, rhodopsins, which
Auxins
bacters can possess either the demethylation pathway support photoheterotrophic growth via the light-driven
A class of hormones that
or the cleavage pathway, and some strains have both77. membrane translocation of protons and sodium ions,
stimulate growth and regulate
the behaviour of phototrophs. Indeed, the roseobacter strain Ruegeria pomeroyi, which may contribute to the formation of electrochemical gra-
has a DMSP demethylase gene (dmdA), as well as three dients and are found in both flavobacterial isolates and
Holdfasts DMSP lyase orthologues (dddP, ddpQ and dddW)77,102, in the SAGs of marine flavobacteria107,110 (FIG. 5). In addi-
Adhesive structures that
is proving to be a valuable strain for studies aimed at tion, proteomic data indicate that rhodopsin is produced
facilitate the attachment of a
cell to a surface. understanding the regulation of DMSP transformation during phytoplankton blooms64. Although it has been
by marine bacteria. proposed that flavobacteria have a bimodal lifestyle, in
Aerobic anoxygenic which they could simultaneously derive energy from the
phototrophy
Flavobacteria. Like roseobacters, flavobacteria are oxidation of organic compounds and light-driven ion-
A photoheterotrophic strategy
found outside phytoplankton blooms. Global ocean pumping rhodopsins107, the extent to which this addi-
in which bacteriochlorophyll a
reaction centres are excited by surveys suggest that flavobacteria are most abundant in tional energy source supports these populations is not
the absorption of light and upwelling, temperate to polar oceans and coastal regions, entirely clear in the context of phytoplankton blooms
pass electrons through a series and that open ocean bacterial communities typically that are rich in organic matter. In addition to the light-
of carrier proteins that pump
contain 10–20% Bacteroidetes, most of which are flavo- driven membrane translocation of ions, a flavobacterium
protons out of the cell, which
contributes to the bacteria103,104. In the context of phytoplankton blooms, rhodopsin that pumps chloride ions was recently char-
electrochemical gradient of the flavobacterial abundance is typically highest during the acterized and is probably involved in the maintenance
cell. decay phase30,55,105, and it has been proposed that a pri- of osmotic balance117.
mary role for members of this group is the conversion The association between phytoplankton and flavo-
Photoheterotrophic
of HMW compounds into LMW compounds17. In fact, bacteria is likely to be more complex than the ability of
A term used to describe a
heterotroph that uses light analysis of the gene content of sequenced isolates106–109, flavobacteria to transform HMW compounds. A key
(that is, photons) to fuel as well as the genomes of uncultured environmental rep- aspect that is required for the efficient degradation of
energy-requiring metabolic resentatives (that is, single amplified genomes (SAGs) particulate matter is the adhesion of bacteria to the sub-
processes.
derived from cells isolated by flow cytometry, but not strate. The production of polymer-degrading enzymes
Fosmid libraries cultivated)110 and fosmid libraries111 predicts that at least that target host cellular components, such as the cell
Libraries of cloning vectors some flavobacteria are better adapted to using complex wall, is a common feature of Bacteroidetes116. Genes that
derived from the bacterial substrates than simple, monomeric compounds112. The encode products that are predicted to be exported out of
F plasmid that stably maintain
ability of flavobacteria to use a broad range of biopoly- the cell and that mediate the breakdown of eukaryotic
large fragments of DNA and
mers, particularly polysaccharides and proteins, as pri- cells, such as proteases, have been found in flavobacteria
are often used for sequencing
or phenotypic screening. mary carbon and energy sources can explain the varied genomes108. In addition, new taxa of flavobacteria that
interactions that these bacteria seem to have not only show microalgicidal activity have been described118,119,
Rhodopsins with eukaryotic phytoplankton but also with marine and several flavobacterial isolates have been found to
Transmembrane proteins that
vertebrates and mammals113. cause disease in macroalgae, particularly red algae120.
function as light-driven ion
pumps; they are present in all Although only a few metatranscriptomic and Another common characteristic of flavobacteria is their
three domains of life. metaproteomic studies, which differ in terms of the ability to move rapidly across surfaces via gliding. The
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Phytoplankton
DOM Motility
adhesin
Membrane- Extracellular
TBDT associated enzyme
system hydrolytic ATP
ATP enzyme ABC-type
ATP transporters
synthase H+
ADP
H+ Rhodopsins Secondary
Na+ transporter
hν
– hν
Cl
hν Adhesins
POM
Virulence
factors
Figure 5 | Physiological features of flavobacteria that facilitate associations with phytoplankton. Flavobacteria
Nature Reviews | Microbiology
genomes encode several physiological processes that probably contribute to their interactions with phytoplankton and
phytoplankton-derived organic matter. These include membrane-associated and extracellular hydrolytic enzymes, such
as laminarinases and β-D-fucosidases, for the degradation of high molecular weight compounds that cannot pass through
bacterial cell membranes. Flavobacteria have highly efficient, multiprotein extracellular systems that bind to large
molecules, enzymatically digest them, and then shuttle the products through dedicated transport systems, such as
TonB-dependent transport (TBDT) systems. Flavobacteria have additional transporters that are both ATP-dependent
(ATP-binding cassette (ABC)-type) and ATP-independent (that is, secondary transporters) that facilitate the uptake of low
molecular weight components of phytoplankton dissolved organic matter (DOM). Some strains have cell surface motility
adhesins, such as SprB and RemA, which are necessary for gliding motility over surfaces. Other surface proteins, which are
predicted to be adhesins owing to the presence of conserved, repetitive peptide motifs, may facilitate attachment to both
living and dead surfaces, such as particulate organic matter (POM). Virulence factors, such as proteases, are encoded in
some flavobacteria genomes and might have algicidal properties. Many flavobacteria genomes also encode rhodopsins
that function as light-driven ion (H+, Cl–, or Na+) pumps. Although their function during phytoplankton blooms has not
been elucidated, H+ and Na+ gradients can be used to drive substrate translocation or ATP production via ATP synthases,
whereas Cl– pumps are probably involved in maintaining an appropriate intracellular ion balance.
specific mechanism of gliding is not fully understood, type A and fasciclin, are also present in many flavobacte-
but it seems to be unique to Bacteroidetes and involves ria genomes110. Finally, flavobacteria seem to be adapted
the production of a ‘slime layer’ of exopolysaccharides to scavenge any energy source that is produced during
and mobile cell surface adhesins (known as SprB and phytoplankton growth, including hydrogen gas, which
RemA in Flavobacterium johnsoniae) that are propelled is produced in the ocean during nitrogen gas fixation123.
by a gliding motor121 (FIG. 5). This trait might facilitate Although the same organisms that fix nitrogen also recy-
the exploration and colonization of growth substrates16 cle hydrogen, some hydrogen is released into the environ-
and might also have a predatory role, as it has been sug- ment, where it could be used as a readily available energy
gested that flavobacteria prey on other bacterioplankton source. Hydrogen uptake genes have been described in
species122. Additional adhesins that have been implicated the SAGs of the environmental flavobacteria MS024-2A
in cell surface and cell–cell interactions, including those and MS024-3C, which may better represent the genetic
that contain peptide motifs that are conserved in all repertoire of flavobacteria than cultivated strains, as
domains of life, such as cadherin, von Willebrand factor indicated by oceanic metagenomic data110.
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Description:plex marine food web, which relies heavily on microbial The remaining carbon either enters the classic .. wall (known as a frustule)133, which is exclusive to diatoms, and structural variations between species yield a . ing and after a bloom have recently been reported17,61. Although phage.
