microbial ecology of anaerobic carbon mineralization in namibian shelf sediments

183 Pages·2008·1.54 MB·English

MMIICCRROOBBIIAALL EECCOOLLOOGGYY OOFF AANNAAEERROOBBIICC
CCAARRBBOONN MMIINNEERRAALLIIZZAATTIIOONN IINN NNAAMMIIBBIIAANN
SSHHEELLFF SSEEDDIIMMEENNTTSS

EELLSSAABBÉÉ MM.. JJUULLIIEESS
MICROBIAL ECOLOGY OF ANAEROBIC CARBON
MINERALIZATION IN NAMIBIAN SHELF SEDIMENTS

Dissertation

zur Erlangung des Doktorgrades
der Naturwissenschaften

-Dr. rer nat.-

dem Fachbereich 5 der Universität Bremen

vorgelegt von

Elsabé Mathilda JULIES

Bremen
2007
Die vorliegende Arbeit wurde in der Zeit von Januar 2004 bis Dezember 2007 am Max-Planck
Institut für Marine Mikrobiologie in Bremen erstellt.

1. Gutachter: Prof. Dr. Bo Barker Jørgensen

2. Gutachter: Prof. Dr. Kai-Uwe Hinrichs

Weitere Prüfer:

Prof. Dr. Wolfgang Bach
Dr. Volker Brüchert

Tag des Promotionskolloquiums: 25. Januar 2008
For my son Stefan
“Microbial ecology is the study of microbial physiology under the
worst possible conditions“(Brock 1966)
Table of Contents
Acknowledgements…………………………………………………………………..……….......I
Summary………………………………………………………………………………………….1
Zusammenfassung………………………………………………………………………….……6
Chapter 1: Introduction 11
The marine carbon cycle……………………………………………………………………..12
The Namibian upwelling system as a highly productive system………………………….....15
Degradation of organic carbon in marine sediments………………………………………...18
Studying the role of Bacteria in organic carbon degradation in marine sediments………….23
Aims and outline of the thesis……………………………………………………………...25
Overview of the manuscripts ……………………………………………………………...41
Chapter 2: 42
Diagenetic transformation of organic matter in Namibian shelf sediments:
Limitation of microbial activity and bacterial abundance
Chapter 3: 87
Characterization of microbial community structure in biogeochemical contrasting shelf
sediments from the Namibian upwelling system
Chapter 4: 128
Microbial response to substrate addition during anaerobic degradation of organic
carbon in Namibian shelf sediment
Conclusions and Perspectives 172
Manuscripts not included in this thesis (abstracts) 174
Acknowledgements
Acknowledgements
This PhD thesis deals with the stepwise degradation of dissolved organic carbon (DOC) in
shelf sediments from the Namibian upwelling system and investigates the processes that control
organic carbon transformation, which ultimately affects the rate and fluxes of hydrogen sulfide
into the water column. It is part of the Geotechnology Program of the Federal Ministry of
education and research, Germany (BMBF) and the German Research Foundation (DFG), Grant
03G0580B Namibia gas (NAMIBGAS). Additional financial support was provided by the Max-
Planck-Society and travel grants were provided by the Benguela Environment Fisheries
Interaction and Training Program (BENEFIT).
I like to thank my advisors Volker Brüchert and Bernhard Fuchs for their time to listen and
reply to a multitude of questions and demands during the laboratory phase and the writing phase
of this thesis. It was not always easy to communicate over thousands of kilometers. I am grateful
to Bo Barker Jørgensen and Volker Brüchert for believing in me and giving me the opportunity
to do my PhD thesis at the Max Planck Institute in Bremen. The experience made me a richer
person. I like to thank the MARMIC research school at the Max Planck Institute for their
assistance during my studies.
I would like to thank Bo Barker Jørgensen and Kai-Uwe Hinrichs for reviewing this thesis.
I am indebted to Carol Arnosti for her assistance, teaching me some of the methods in her
laboratory in Chapel Hill, and her input in the first manuscript. I like to thank Katharina Kohls
and Nina Knab for commenting on some parts of the thesis. Thanks to Elke Busch and Ulrich
Busch for helping with the translation of the summary.
The crew of the RV Alexander von Humboldt and the RV Welwitchia are thanked for their
assistance during sampling. I like to thank the scientists and technicians at the National Marine
I
Acknowledgements
Information and Research Center (NATMIRC) for their assistance and understanding during my
visits in Namibia. Without the study leave granted by the University of Namibia, my stay and
studies in Bremen would have been impossible. Therefore I like to express my deepest gratitude
to my colleagues in the Department of Biology at the University of Namibia for their
understanding and support during my studies.
All my fellow PhD students and my friends at the Max Planck Institute, thank you for your
friendship and all the fun we had during our studies.
To my parents, thank you for your support even if you never really understood why I have to
play with mud again in my adult life. Thank you ma and pa for many days of baby sitting and for
taking such good care of what is the most important to me, my son. I also like to thank my sisters
for their friendship and support.
“Behind every successful woman is a successful man”. I am extremely lucky and happy to
have two successful and brave men supporting and loving me. Thank you Stefan for your
understanding when I had to leave you for three years to pursue my studies you are the bravest
boy. Mommy loves you very much. Thank you Uli for your love and for being not only my
partner, but also my biggest fan, supporter, friend, and mentor.

II
Summary
Summary
This PhD thesis is an essential component of the “Namibia Gas” (NAMIBGAS) project,
which aims to improve the understanding of the rate and fluxes of hydrogen sulfide and methane
to the sediment surface and into the water column on the Namibian shelf, which is one of the
most productive upwelling systems on Earth. Organic matter degradation in the sediment drives
hydrogen sulfide production, the maintenance of anoxia, and methane formation. Therefore, the
primary aims of the thesis are to study carbon transformation processes within the sediment,
determine the reactivity of organic carbon in the sediment and, investigate the control of
microbial community structure and activity by the amount and accessibility of carbon sources.
The emphasis is on linking microbial community structure (identity) to their function (activity)
to provide new insights into the microbial ecology that controls carbon turnover in these
upwelling sediments. By studying the stepwise degradation of organic carbon a complete process
overview of organic carbon mineralization could be obtained.
Firstly, the diagenetic transformation of dissolved organic carbon (DOC), in particular
dissolved carbohydrates, was studied by using both biogeochemical methods and molecular
techniques. The bulk sediment composition, pore water chemistry, polysaccharide hydrolysis
rates, 35S-sulfate reduction rates, and the abundance of active bacteria involved in the initial and
terminal processes of organic carbon degradation within the top 15 cm of the sediment from two
sampling stations were determined (Chapter 2). Secondly, the diversity of bacteria from the same
two sampling stations within the top 12 cm of the sediment, using the 16S rRNA library
approach were investigated (Chapter 3). The central question was whether shifts of the
community structure of bacteria involved in the major carbon transformation steps of hydrolysis,
fermentation, and terminal oxidation are reflected in changes of biogeochemical rates. Finally,
1
Summary
the effect of a sudden high input of DOC into the sediment in the form of high molecular weight
substances (the polysaccharide laminarin) and low molecular weight substances (lactate and
acetate) on the metabolic activity and community structure of bacteria involved in initial
hydrolytic and fermentation steps and terminal oxidation was investigated during two separate
experiments (Chapter 4). Substrate addition simulates the high input of organic matter into the
sediment after a phytoplankton bloom, following upwelling events.
In the different experiments performed in this thesis, only two structurally specific
polysaccharides, laminarin and pullulan were used as proxies of carbohydrates to quantify the
initial transformation of high molecular weight DOC in Namibian shelf sediments, because of
the complexity of DOC and the limited methodology for its characterization.
A tight coupling between the active heterotrophic and sulfate-reducing bacterial communities
existed in the top 10 cm of the sediment, which is reflected in the low volatile fatty acid (VFA)
concentrations. The coupling between initial steps and terminal oxidation appears to be
controlled by the availability of degradable dissolved organic matter. Gradients in
biogeochemical rates and bacterial abundance were not reflected in the depth profiles of
particulate organic carbon (POC), DOC, VFA, or total dissolved carbohydrates. This is because
an increasing amount of DOC, including the carbohydrate fraction, became unavailable to
microbial communities with depth, resulting in an increasing substrate limitation for the active
bacteria with depth. The shift in the microbial community composition with depth as revealed by
16S rRNA clone libraries was due to the decrease in organic carbon substrate availability, which
results in niche diversification that is related to the physiological abilities of the microorganisms.
Experiments in which the sediment was amended with organic carbon also revealed that
microorganisms in the top 6 cm of the sediment and in the bottom sediment (14-16 cm depth)
2