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Diversity, salinity adaptation, and role in carbon cycling of microbial communities inhabiting the oxic layer of intertidal hypersaline microbial mats [Elektronische Ressource] / vorgelegt von Katharina Kohls

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Published 01 January 2010
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Diversity, salinity adaptation, and role in

carbon cycling of microbial communities

inhabiting the oxic layer of intertidal
Title page shows hypersaline microbial mats from the upper intertidal flat of the hypersaline microbial mats
Arabian Gulf coast at Abu Dhabi (UAE). The red mat is lying in a channel and is
always covered with seawater, whereas the grey mat is completely dry and cracked
into polygons.
Katharina Kohls








































Title page shows hypersaline microbial mats from the upper intertidal flat of the Arabian
Gulf coast at Abu Dhabi (UAE). The red mat is lying in a channel and is always covered
with seawater, whereas the grey mat is completely dry and cracked into polygons. Diversity, salinity adaptation, and role in
carbon cycling of microbial communities
inhabiting the oxic layer of intertidal
hypersaline microbial mats








Dissertation zur Erlangung des Doktorgrades der Naturwissenschaften

-Dr. rer. nat.-

dem Fachbereich Biologie/Chemie der Universität Bremen vorgelegt von







Katharina Kohls







Bremen
Mai 2010
Die vorliegende Arbeit wurde am Max-Planck-Institut für marine Mikrobiologie in
Bremen angefertigt.
























Gutachter:

Prof. Dr. Friedrich Widdel
Dr. Dirk de Beer


Prüfer:

Prof. Dr. Ulrich Fischer
Dr. Raeid M. M. Abed


Tag des Promotionskolloqiums: 05. Juli 2010 Table of contents

Summary………………………………………………………………………………... 1
Zusammenfassung…………………………………………………………………….... 3

Part I: Combined presentation of results

7 A Introduction…………………………………………………………………………
1. Microbial mats………………………………………………………………. 7
2. Cyanobacteria and aerobic heterotrophic prokaryotes in microbial mats
-Autotrophy and Heterotrophy- …………………………………………….. 9
3. Intertidal microbial mats of Abu Dhabi …………………………………….. 12
4. Salinity adaptation strategies of microorganisms in microbial mats………... 15
5. Methods………………………………………………………………………. 16
16 5.1 Molecular tools…………………………………………………......
17 5.2 Microsensors………………………………………………………..
6. Objectives of this thesis………………………………………….…………... 19

21 B Results and Discussion……………………………………………………………..
1. Effects of salinity on microbial behavior, metabolism, and community
21 structure……………………………………………………………………...
21 1.1 Salinity-driven migration of cyanobacteria – “Halotaxis”………….
1.2 Effect of salinity on oxygen consumption and photosynthesis ……. 23
1.3 Effect of salinity on microbial diversity……………………………. 24
2. Interaction between cyanobacteria and aerobic heterotrophs……................... 26
2.1 Diversity and abundance of aerobic heterotrophic prokaryotes in
hypersaline microbial mats………………………………................ 26
2.2 DNA-SIP to identify key aerobic heterotrophic prokaryotes
involved in carbon cycling using an intact microbial mat …………. 28
2.3 Cyanobacterial monocultures as model systems………………….... 29 C Final discussion………………………………………………………………….. 31
1. Adaptation strategies of microorganisms to extreme conditions………….. 31
2. Aerobic heterotrophic prokaryotes in the Abu Dhabi mats……………….. 33
3. Microbial consortia in extreme environments: Interaction between
aerobic heterotrophic prokaryotes and cyanobacteria……………………... 34
37 4. Relevance of studying microbial communities in extreme habitats………..
5. Conclusion and outlook…………………………………………………... 38

D References………………………………………………………………………… 39

Part II: Publications

55 A List of Publications……………………………………………………………….
I. Publications presented in this thesis……………………………………….. 55
II. Publications not presented in this thesis…………………………………... 56

B Publications……………………………………………………………………….. 61
1. Halotaxis of cyanobacteria in an intertidal hypersaline microbial mat........ 61
2. Effect of salinity changes on the bacterial diversity, photosynthesis and
oxygen consumption of cyanobacterial mats from an intertidal flat of the
71 Arabian Gulf……………………………………………………………….
3. Lipid biomarkers, pigments and cyanobacterial diversity of microbial mats
across intertidal flats of the arid coast of the Arabian Gulf
(Abu Dhabi, UAE)…………………………………………………………. 83
4. Abundance and community composition of Bacteria and Archaea in the
99 oxic layer of a hypersaline intertidal cyanobacterial mat………………….
5. Molecular identification of aerobic heterotrophic bacteria in hypersaline
microbial mats and their interaction with associated cyanobacteria……... 129
Danksagung……………………………………………………………………….. 157

Eidesstattliche Erklärung………………………………………………………… 159 Summary

Summary

The main objective of this thesis was to study the diversity, salinity adaption, and role in
carbon cycling of microorganisms inhabiting the oxic layer of intertidal hypersaline
microbial mats. For this purpose, mats from the Arabian Gulf coast of Abu Dhabi, United
Arab Emirates (UAE), which are subjected to multiple harsh environmental conditions of
temperature, UV and light intensity, salinity and salinity fluctuations, as well as
desiccation, were investigated.
In the first study (publication 1), a new salinity-driven taxis of cyanobacteria in
the upper tidal mat was discovered and termed as ‘Halotaxis’. Microcoleus
chthonoplastes filaments migrated up and down when salinity was decreased below or
increased above 15%, respectively. The migration caused a color change of the mat’s
uppermost layer from red to green and vice versa. We assume that this migration has a
protective function for cyanobacteria inhabiting environments that are exposed to strong
salinity fluctuations (e.g. intertidal microbial mats), since the bacteria always migrated to
lower salinities. Furthermore, a decrease of photosynthesis and oxygen consumption rates
at salinities higher than 10% was shown in a low, middle, and upper tidal mat
(publication 2). In the upper mat, which was exposed to the highest salinities as well as
salinity fluctuations (i.e. from 6 to 20%), the extent of inhibition of these processes
turned out to be lower, indicating a more efficient salt adaptation of the resident
microorganisms. Interestingly, this mat possessed the highest bacterial diversity.
Probably, the resistant fraction of the original community was not affected, whereas the
growth of halophilic bacteria was promoted, leading to an increased biodiversity. A
further study showed that the mats’ microorganisms also possessed adaptation
mechanisms to strong desiccation, high UV and light intensities, and high temperatures
(publication 3).
The upper tidal mat was further investigated with respect to the composition and
role in carbon cycling of aerobic heterotrophic prokaryotes (AHP). This mat hosted a
novel and unique diversity of potential AHP. Sequences related to ones of Chloroflexi-
like bacteria, Bacteroidetes, Proteobacteria, Haloarchaea, and Crenarchaeota dominated
the clone libraries of the uppermost oxic part of this mat (publication 4). Among the
1Summary

sequences, many extremophilic (mainly halophilic) bacterial and archaeal genera, such as
e.g. Deinococcus, Salinibacter, and Halobacteria were found. Since cyanobacteria live in
close proximity to aerobic heterotrophs, we further investigated the interactions between
the two groups (publication 5). DNA-stable isotope probing revealed a higher activity of
unicellular cyanobacteria with regard to CO fixation, compared to filamentous 2
13cyanobacteria. A specific and clear C-labeling of aerobic heterotrophic bacteria (AHB)
was not evident, most likely due to methodological artifacts. However, the results hinted
to the potential importance of Chloroflexi-like bacteria, Bacteroidetes, and
Proteobacteria in carbon cycling. Investigations of unialgal cyanobacterial cultures as
model systems indicated that the community structure of associated AHB is species-
specific and depends on the environment, from which the culture was obtained.
Interestingly, a community of cyanobacteria-associated AHB or rather their released
substances apparently stimulated growth of their natural host, but inhibited other
cyanobacterial strains, thereby enhancing the host’s competitiveness. The advantage for
associated bacteria might be the supply with certain cyanobacterial exudates, vitamins, or
growth factors. These interactions are manifold, very complex, highly specific, and
provide high potential for biotechnological purposes, e.g. for the discovery of new
bioactive substances.
2