Environmental, biogeographic and biochemical patterns of Archaea from family Ferroplasmaceae

30 Pages·2011·5.38 MB·English

AEM Accepts, published online ahead of print on 17 June 2011
Appl. Environ. Microbiol. doi:10.1128/AEM.00726-11
Copyright © 2011, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.
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3 Environmental, biogeographic and biochemical patterns of Archaea
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4 from family Ferroplasmaceae n
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7 //a
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8 Olga V. Golyshina1 a
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9 1School of Biological Sciences, Bangor University, LL57 2UW Gwynedd, Wales, g
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10 UK D
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12 Running title: Family Ferroplasmaceae
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13 Keywords: Ferroplasmaceae, acidophilic Archaea, iron oxidation 8
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15 Correspondence: [email protected]
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2 About ten years ago a new family of cell-wall deficient, iron-oxidizing archaea,
3 Ferroplasmaceae, was described within the large archaeal phylum of Euryarchaeota. In this
4 minireview I summarize the research progress achieved since then and report on the
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5 current status of taxonomy, biogeography, physiological diversity, biochemistry and other w
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6 research areas involving this exciting group of acidophilic Archaea. a
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7 fr
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9 Microorganisms thrive remarkably well under various conditions including high temperatures, e
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10 extremely high osmosis and very acidic pH that would generally be considered as hostile or s
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11 limiting to higher organisms. Studies of, and understanding the, uniqueness of extremophilic o
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12 organisms and biochemical and cellular processes underlying their functioning and their role in o
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13 biogeochemical processes comprise an emerging research area in modern bioscience. Of a e
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14 special interest for various biotechnological applications are enzymes produced by m
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15 extremophiles, the so-called extremozymes, that exhibit a high activity and stability under r
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16 extreme physical-chemical conditions. The representatives of the “third domain of life”, the 2
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17 archaea are unique contributors to this area of special interest. Several factors make the archaea 8

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18 an attractive subject to study including their: relatively recent history of discovery, ability (often g
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19 much higher than that in bacteria) to adapt to harsh environments, enigmatic nature and low s
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20 cultivability.
21 This minireview focuses on acidophiles representing the euryarchaeal family Ferroplasmaceae
22 first described about a decade ago (25) and on some aspects relevant to their physiology,
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1 geographic distribution and taxonomic diversity. Representatives of this family are cell wall-
2 lacking extreme and obligate acidophiles that are able to grow at pH values around 0. Together
3 with their closest phylogenetic neighbors from the family Picrophilaceae they comprise a group
4 of the most extreme acidophilic organisms known. Furthermore, Ferroplasmaceae thrive in
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5 systems with high concentrations of iron, copper, zinc and other metals. Archaea of the family o
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6 Ferroplasmaceae co-exist in their natural habitats with other acidophilic or acid-tolerant lo
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7 prokaryotes, namely with the members of bacterial phyla Firmucutes, Proteobacteria, e
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8 Actinobacteria, Nitrospirae, representatives of Crenarchaeota and other Euryarchaeota that are o
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9 important drivers in environmental acid generation and in global cycling of iron and sulfur. t
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10 Accordingly, being important iron-oxidizers, the organisms of the family Ferroplasmaceae /a
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11 significantly contribute to these processes. .
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12 Biogeography The members of the family Ferroplasmaceae are distributed world-wide (Fig. 1) .o
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13 and can be found in a variety of acidic environments with very stable chemical conditions such o
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14 as ore deposits, mines, acid mine drainage systems (natural or man-made) and in areas with
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15 geothermal activity. Detection or quantification of Ferroplasmaceae in these environments were m
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16 done mostly using SSU rRNA-targeting analyses such as 16S rRNA gene clone libraries’ r

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17 sequencing, amplified ribosomal DNA restriction analysis (ARDRA) profiling, real-time ,
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18 quantitative PCR, restriction fragment length polymorphism (RFLP) or fluorescence in situ 8

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19 hybridization (FISH) and oligonucleotide microarray analysis, all of which revealed the presence
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20 of these archaea in a number of pyritic/arseno-pyritic, gold-arseno-pyritic/chalcopyritic, led-, s
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21 zinc- and copper-containing mines across all continents (11, 24, 26, 45, 46, 51, 55, 56, 57, 58).
22 Clones related to family Ferroplasmaceae have also been documented in further natural sulfides-
23 rich ecosystems: e.g. in the snottites, i.e. the stalactites-like formations of microbial origin taken
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1 from walls of Frasassi Cave and in the Rio Garrafo cave systems both located in Italy where
2 acidic microenvironments were formed as a result of sulfide oxidation (38). Acid mine drainage
3 systems of Richmond mine on Iron Mountain (Ca, USA) and Rio-Tinto (Spain) have been
4 extensively studied as environments hosting Ferroplasmaceae (1, 3, 18, 23, 29). For years the
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5 family Ferroplasmaceae was represented by a single monospecific genus Ferroplasma o
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6 containing only a single species with a validly published name, F. acidiphilum YT DSM 12658T lo
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7 (25). Further isolates belonging to the genus Ferroplasma have been obtained, such as e
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8 “Ferroplasma acidarmanus” fer1 (18) and few others, with SSU rRNA identical to that of F. o
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9 acidiphilum or just with few mismatches (12, 16, 40, 41; Johnson, personal communication) t
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10 (Fig. 2). A new genus Acidiplasma of the family Ferroplasmaceae has very recently been /a
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11 described to contain two species named Acidiplasma aeolicum VT (DSM 18409T=JCM 14615T) .
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12 and A. cupricumulans (DSM 16551T = JCM 13668T) isolated from the hydrothermal pool located m
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13 on Vulcano Island (Italy) and from chalcocite/copper containing heaps (Myanmar), respectively g/

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14 (28, 30, 31). A few other Acidiplasma-like strains have been isolated from pyrite and
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15 chalcopyrite-leaching bioreactors (59). It should also be noted that A. aeolicum is not the only e
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16 representative of the family Ferroplasmaceae isolated from sites with high geothermal activity, e
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17 rich in ferrous sulfides, hydrogen sulfides and sulfur dioxide. There is quite a number of similar 4
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18 moderately thermophilic strains isolated in our laboratory from South Europe’s stratovolcanos 01
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19 with high hydrothermal activity observed on the sites in forms of hot springs along the costs, by

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20 solfataras and fumaroles (Fig. 3). ue
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21 Sequences of archaea of family Ferroplasmaceae were also recovered from Red Sea samples
22 taken from Atlantis II, the world-largest marine polymetallic ore body (Abdallah, personal
23 communication). Many questions arise in connection with these local environmental conditions
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1 as atmosphere, salinity, pH range and general features of sea water promoting buffering capacity.
2 However, the findings summarized above undoubtedly represent only a very small proportion of
3 still undetected and uncharacterized family members.
4 In seeking an explanation for why the Ferroplasmaceae are so globally ubiquitous (which is
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5 reflected in numerous literature references and sequence databases’ entries), one might consider w
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6 the global abundance of iron, which is the fourth-abundant chemical element on the Earth crust a
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7 and is found in concentrated deposits are widely distributed across all continents. Iron-containing
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8 mineral pyrite is the most ubiquitous sulfide mineral on Earth, accumulated in sites of m

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9 hydrothermal origin and found in ingneous, sedimentary and metamorphic rocks. It is quite tp
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10 obvious that different acidic ecosystems with extremely low or moderately-valued pH and high e
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11 concentrations of iron favorable to iron-oxidizing acidophiles exist in many locations on our a
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12 Planet. It may also be suggested that there is a sampling bias that favours acid mine drainage .o
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13 (AMD) systems or ore deposits because of biotechnological/commercial importance and their o
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14 contribution to the environmental pollution. Indeed, AMD streams are the cause of a significant
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15 negative impact on the surrounding ecosystems due to their contribution of highly acidic waters m
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16 containing high concentrations of toxic soluble metals to the rivers, seas and oceans. Further, r

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17 volcanic acidic environments associated with tectonic activities are another sampling “hotspot” ,
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18 and attract an increasing attention of microbiologists who seek unusual microorganisms and an 8

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19 understanding of their biogeochemical activities. Vulcano Island is an example of an extensively
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20 sampled, yet un-exhausted geothermally active site, where about a few dozens of new species of s
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21 thermophilic archaea and bacteria have already been isolated and described. On the other hand, a
22 feasible explanation for the occurrence of Ferroplasmaceae in such environments with relatively
23 consistent conditions, in terms of pH and high concentrations of soluble iron, are their relatively
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1 small genomes pre-determining metabolism and narrowing their niche as discussed earlier (26).
2 Ferroplasmaceae exhibit a combination of physiological traits compared to other acidophilic
3 prokaryotes that will further be discussed in details in the section “Physiological variability
4 within Ferroplasmaceae”.
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5 It is interesting to mention that the strains VT (A. aeolicum) and BH2T (A. cupricumulans) o
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6 isolated from geographically distinct regions and from geologically and geochemically distinct lo
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7 ecosystems (Vulcano Island (Italy) and mine in Myanmar; acidic volcanic pool and chalcocite- e
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8 and copper-containing ore, correspondingly) exhibit no mismatches in their 16S rRNA gene o
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9 sequence, however the results of DNA-DNA hybridization revealed that the strains indeed t
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10 belong to two different species (28). /a
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11 The same is also true for many Ferroplasmaceae isolated from various locations (Fig. 3): most .
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12 members of Ferroplasma spp. (16) and Acidiplasma spp. exhibited identical 16S rRNA gene
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13 sequences within corresponding genera. This does not necessarily mean that all strains belong to g/

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14 same species and are not distinct physiologically since the natural variability of mineral
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15 substrates, pH, different types of ores etc. in isolation sites representing a very powerful natural e
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16 force for evolution and speciation. e
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17 In the past few years numerous examples of uncultured Thermoplasmatales, the so-called ,
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18 “Alphabet-plasmas”, detected in clone libraries or found in metagenomic sequencing datasets 8

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19 derived from a great variety of environments, have emerged (3, 38, 45; to name few). SSU rRNA
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20 gene sequences of “Alphabet-plasmas” have a very broad phylogenetic diversity across the order s
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21 Thermoplasmatales. It is not clear if the epithet “plasma” is appropriate in the context of cellular
22 morphology, i.e. whether these organisms lack the cell wall, since even within
23 Thermoplasmatales, the archaea from genus Picrophilus spp. have a rigid cellular envelope (49,
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1 50) and thus cannot be considered as “–plasmas”. I therefore believe to avoid further confusion
2 these organisms must be defined as “members of Thermoplasmata/Thermoplasmatales” or other
3 taxon, depending on their affiliation within a commonly recognized taxonomic boundary.
4 Physiological variability within Ferroplasmaceae All members of the family
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5 Ferroplasmaceae, with minor exceptions, share quite similar physiological traits which, at some o
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6 extent, makes it difficult to distinguish isolates for provision of taxonomic descriptions. lo
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7 According to the opinion of Valentine (53), the physiology and phylogeny are generally more e
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8 cohesive in archaea than in bacteria. For example, Valentine places the physiologically coherent o
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9 halophilic archaea that form a phylogenetically tightly clustering group of 22 genera within just t
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10 one class known as Halobacteria which is in a sharp contrast to phylogenetically diverse /a
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11 halophilic bacteria that span more than 10 different classes of Bacteria. All members of the .
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12 family Ferroplasmaceae that have been physiologically characterized share extreme acidophily
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13 (optimal pH range of 0.8-1.8), ubiquitous capacity for ferrous iron oxidation (within this family g/

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14 there are no isolates known that are unable to oxidize ferrous) and a strict dependence on low
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15 concentration of yeast extract, common for a vast majority of archaea. Some variations among e
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16 strains of the two genera comprising Ferroplasmaceae are known in the relation to the ability for e
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17 chemoorganotrophy, aerobic or facultative anaerobic growth or temperature growth optima 4
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18 (mesophilic or moderately thermophilic). Mesophilic or moderate thermophilic Ferroplasmaceae 01
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19 exhibit growth at optimal temperatures from 35 ºC for the most mesophilic strains to 55 ºC for by

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20 the majority of thermophilic isolates. Being able to outperform the competitors at moderate ue
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21 temperatures or across a relatively wide temperature range is an important option for these iron-
22 oxidizers as iron/pyrite oxidation is an exothermic process. CO fixation rates in F. acidiphilum
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23 strains YT and Y-2 were reported to be relatively low, approximately 12 times lower than those
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1 in optimally-grown, iron-oxidizing bacterium Acidithiobacillus ferrooxidans (41), a margin
2 similar to that observed for growth rates which are generally low in all Ferroplasmaceae (16,
3 25). However, Acidiplasma aeolicum VT grown chemoorganotrophically on glucose and yeast
4 extract, while exhibiting lower growth rates, produces higher biomass yields per unit of
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5 consumed substrate (28). Karavaiko and co-authors (34) suggested that the occurrence of more o
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6 diverse variants of metabolism, e.g. mixotrophy and general reduction of autotrophy in lo
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7 environments with higher temperatures is a function of the lower solubility of both oxygen and e
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8 CO required for iron oxidation and autotrophy. Heterotrophic metabolism in some members of o
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9 Ferroplasmaceae may function as an ecological advantage enabling this group to operate like t
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10 Thermoplasma spp., by scavenging organic matter produced in microbial biofilms that are /a
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11 typically formed in iron-based natural environments. .
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12 Most of the strains of Ferroplasmaceae (majority of F. acidiphilum strains, A. cupricumulans
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13 BH2, A. aeolicum V and further strains of A. aeolicum (Golyshina et al., unpublished)) have been g/

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14 found and isolated from solid ores and minerals, volcanic soils, ash particles, sand/gravel
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15 samples, or from biofilms and microbial mats (e.g. “F. acidarmanus” fer1 (18)), indicating that e
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16 the solid-phase-attached, rather than planktonic cell forms are prevalent in nature. In this e
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17 relation, high levels of adhesion of F. acidiphilum YT cells to the surface of pyrite at acidic 4
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18 conditions was studied and explained through the prism of Deryagin-Landau-Verwey-Overbeek 01
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19 (DLVO) theory, i.e. considering the interaction of two charged surfaces via a thin liquid layer by

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20 (19). Two different types of biofilm morphology have been found produced by the strain ”F. ue
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21 acidarmanus” fer1, and further prevalence of anaerobic type of metabolism has been observed in
22 mature biofilms (7). However, no common quorum sensing signaling molecules have been
23 detected by the authors in the aqueous phase of bioreactors. Given Ferroplasmaceae are non-
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1 motile, they may not necessarily require an extra chemical signal to adhere. Additional studies
2 will be of a great importance for further understanding the mechanisms and kinetics of cellular
3 attachment of Ferroplasmaceae to solid surfaces.
4 Lipid biomarkers. Archaeal tetraether-based lipids are considered to play a pivotal role in
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5 maintaining pH gradient across the cellular membrane (36, 54). The chemical composition of w
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6 membrane lipids is therefore a relevant, if not the only useful marker for chemotaxonomy in a
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7 those archaea. Major membrane lipids of the family members are dibiphytanyl-based tetraether
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8 lipids. The polar lipids were reported to be mostly single phosphoglycolipid derivatives based on m

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9 a galactosyl dibiphytanyl phosphoglycerol tetraether, with minor amounts of mono- and tp
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10 diglycosyl dibiphytanyl ether lipids; and the main respiratory quinones were found to be e
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11 naphthoquinone derivatives (8, 28). F. acidiphilum YT and Y-2 have been reported to have a β- a
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12 D-glucose moiety in their major glycosyl dibiphytanyl phosphoglycerol lipid (8) whereas the .o
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13 sugar residue in A. aeolicum VT was reported to be the β-galactopyranose (28). Undoubtedly, it o
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14 is hard to over state the role of chemotaxonomy in provision of an unambiguous identity of new
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15 isolates for their affiliation at the level of a genus within Ferroplasmaceae and within m
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16 hierarchically higher taxonomic divisions, especially as a result of poor resolution of SSU rRNA r

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17 within a single genus. ,
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18 Viral control in acidophilic microbial communities. Microbial life in acidic ecosystems is b
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19 controlled by factors similar to those in any other microbial community: competitive u
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20 interactions, predation, syntrophic and mutualistic interactions, to name a few (32). Viruses seem t
21 to play an important role in environments populated by Ferroplasmaceae. In some acidic
22 systems, e.g. geothermally active sites, temperatures above 80o C have been known to have lower
23 numbers of viruses in comparison to their abundance in other ecosystems due to challengingly
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1 low pH and high temperatures. Nonetheless, even under such extreme conditions viruses can
2 effectively control microbial densities significantly influencing biogeochemical cycles and acting
3 as drivers of microbial evolution (43, 47). At least two viral morphotypes and virus-host
4 associations have been observed in a cryoelectron microscopy study of ultra small archaeal
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5 “ARMAN” cells from biofilm samples from the Richmond Mine at Iron Mountain (California) o
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6 (13). A further confirmation of the presence of viruses in the environments populated inter alia lo
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7 by members of Ferroplasmaceae is referred to the documentations about presence of sequences e
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8 of CRISPR, CRISPR-associated cas genes and prophage-associated genes identified in the o
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9 process of metagenomic data mining from samples from Richmond Mine (Iron Mountain) by the t
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10 group of Banfield. CRISPR-containing loci were initially identified in large metagenome /a
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11 assemblies to harbour approx. 2400 unique spacer regions that were further compared to all .
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12 contigs and unassembled reads. After that, the spacer-based reconstruction of genome fragments
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13 of viruses was performed and finally, the pairing matches between hosts and viruses were g/

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14 established. The observed prevalent matching of only very recently acquired spacers to
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15 corresponding viruses suggested a high rate of resistance emergency in acid mine drainage e
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16 systems (2, 15). About 24 putative prophage-associated genes have been identified in the e
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17 genome of the strain “F. acidarmanus” fer1; prophage-associated genes were also present in the 4
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18 8 Mbp metagenomic sequencing dataset obtained by shotgun sequencing of small-insert libraries 01
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19 derived from the DNA sample from Richmond Mine, importantly, from the isolation site of the by

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20 strain “F. acidarmanus” fer1 (1). Analysis showed that the gene insertion and loss of genes, ue
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21 possibly of the phage origin, and the presence of numerous transposases are important factors for
22 increasing heterogeneity within the local population (1).