Phylogeny and diversity of symbionts from whale fall invertebrates [Elektronische Ressource] / vorgelegt von Caroline Verna

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• Biologie

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• Publié par: universitat_bremen
• Publié le: 01 janvier 2010
• Nombre de lectures: 19
• Langue: English
• Poids de l'ouvrage: 19 Mo

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Phylogeny and diversity of symbionts from
whale fall invertebrates
Dissertation zur Erlangung des Th`ese de Doctorat de
Grades eines Doktors der l’Universit´e Pierre et Marie
Naturwissenschaften Curie
– Dr. rer. nat. –
Sp´ecialit´e
dem Fachbereich Diversit´e du Vivant
Biologie/Chemie
Pr´esent´ee par
der
Caroline VernaUniversit¨at Bremen
Pour obtenir le grade de
vorgelegt von
Docteur de
Caroline Verna
l’Universit´e Pierre et Marie
am Curie
8. April 2010
Soutenu le
8 Avril 20102Die vorliegende Arbeit wurde in der Zeit von September 2006 bis April 2010 in der
Symbiose-Gruppe am Max-Planck-Institut fur¨ marine Mikrobiologie in Bremen angefer-
tigt. Cette th`ese a ´et´e effectu´ee de Septembre 2006 a` Avril 2010 au Max Planck Institute
for Marine Microbiology dans le groupe Symbiose.
1. Gutachterin/Rapporteur et Directrice de th`ese: Dr. Nicole Dubilier
2. Gutachter/Rapporteur: Prof. Dr. Ulrich Fischer
3. Gutachterin/Rapporteur: Prof. Dr. Monika Bright
4. Gutachter/Rapporteur: Prof. Dr. Daniel Prieur
5. Prufer/Directrice¨ de th`ese: Prof. Dr. Fran¸ coise Gaill
6. Prufer/Examinateur:¨ Prof. Dr. Nadine Le Bris
7. Pr¨ Prof. Dr. Wilhelm Hagen
8. Studentin/´etudiante: Hannah Marchant
9. Mitarbeiterin/employ´ee: Cecilia Wentrup
Tag des Promotionskolloquiums/Jour de la soutenance: 8. April 2010 / 8 Avril 2010
Auf dem Deckblatt, Osedax mucofloris und Symbionten. Links, Wurm in situ Foto (von
A. Glover). Mitte, Schema zeigt die Verteilung der Symbionten. Rechts, Photo der Sym-
bionten mit FISH. / Sur la page de couverture: Osedax mucofloris et symbiontes. Gauche,
photo in situ du vers (par A. Glover). Milieu, schema montrant la distribution des sym-
biontes. Droite, photo des symbiontes r´ealis´ee avec FISH.
34‘Well may we affirm that every part of the world is habitable! Whether lakes of brine, or
those of subterranean ones hidden beneath volcanic mountains—warm mineral
spring—the wide expanse and depths of the ocean—the upper regions of the atmosphere,
and even the surface of perpetual snow—all support organic beings.’
Charles Darwin - The Voyage of the Beagle
5Aknowledgments
Thanks to...
Nicole, For giving me the opportunity to do this thesis. We may not have agreed all
along this work but you listened and supported me until the end. For getting excited about
my results and pushing me to go on when I thought I was stuck and for not letting me
drown in this thesis. For beliving in me more than I did myself. And specially for teaching
me all you did. I hope I will go on in research and improve the skills you helped me develop.
Fran¸ coise Gaill, Merci d’avoir accept´e de superviser ma th`ese malgr´e les difficult´es ad-
ministratives et la distance g´eographique. Ainsi que d’avoir continu´e`a me soutenir malgr´e
vos nouvelles obligations.
The Jury: Dr. Nicole Dubilier, Prof. Dr. Ulrich Fischer, Prof. Dr. Monika
Bright, Prof. Dr. Daniel Prieur, Prof. Dr. Fran¸ coise Gaill, Prof. Dr. Nadine
Le Bris, Prof. Dr. Wilhelm Hagen, For making this double degree possible, and your
feedback on my work.
Marie Donatien, Merci infiniment. Sans vous je n’aurai jamais r´eussi `a vaincre le mon-
stre administratif de P6.
Christiane, We did it! Thank you for all the administrative support. I think we should
both get an additional PhD in how to fight and win administration.
Silke, I wish I could write in German but I cannot. If it were not for your permanent and
wonderful support in the lab I would not have make it. You are a lab superhero and saved
me more times than I can remember. I might have been the unluckiest person in the lab
but you are the best, so thanks again and again for being there and teaching me. Vielen
Dank!
The “Osedax team”, specially Adrian, Thomas, Craig, Helena, Kirsty and Nick. I will
never forget the sampling in Tj¨ arn¨ o, or the smell of decaying whale. If I had to it again I
6would. Thank for sharing your science enthusiasm.
The mollies, my office mates, MPI colleagues, You are wonderful people. I have
enjoyed working with you. I already miss the ones who left and I will miss the atmosphere
once I leave. There was always someone available to help, to chat, have a coffee break and
more. Special thanks to Bernd for allways finding any article I needed.
The Symbiosis group, all present and past members. Most of you are my friends in
addition to wonderful colleagues. Some special thanks to Karina, Judith, Lisa, Dennis,
Claudia, Julie, S´ebastien, Manuel, Christian, Christian and to Jill and C´ecilia for reading
more of this thesis than should have been healthy.
Mme Secchi, Pour m’avoir fait aimer la Biologie.
Ma famille, Merci de m’avoir encourag´e toujours, d’ˆetre l`a quand j’ai besoin de vous, de
croire que je suis une personne formidable. Je vous aime tr`es tr`es fort.
Friends in Bremen, Paris and elsewhere. You are great and you should know it! I
cannot make a list this would to much look like facebook! Merci a` tous, amis de Bremen,
Paris et ailleurs. Vous ˆetes formidables et vous le valez bien. Pas de liste, on est pas sur
Facebook.
The Girls, To the next “girls”evening!
Laura and Jana, Very big hugs! Finally, we will all make it soon and we won’t need plan
B: open a cocktails bar. This 4 years would not have been fun without you.
Doudou, Oui tu m´eriterais un diplˆ ome suppl´ementaire pour valider ta demi-th`ese en mi-
crobiologie marine. Merci des millions de fois.
78Abstract
When whales die and sink to the seafloor, their decaying carcasses form oases at the bot-
tom of the ocean that provide an energy source for a highly diverse and abundant fauna
thriving at these unusual and ephemeral habitats. Among these species some are associ-
ated with chemoautotrophic symbionts, and were initially known from hydrothermal vents,
cold seeps and wood falls, such as vestimentiferan tubeworms, bathymodiolin mussels, and
vesicomiyd clams. In addition to these chemoautotrophic symbioses, a new symbiosis type
was discovered with heterotrophic bacteria: Osedax worms are whale fall specialists that
infiltrate whale bones with their root tissues. These roots are filled with endosymbiotic
bacteria hypothesized to provide their hosts with nutrition by extracting organic com-
pounds from the whale bones (i.e. heterotrophic bacteria). Although whale falls are a
suitable habitat for different symbioses (chemoautotrophic and heterotrophic), symbiosis
at whale falls remains mostly unexplored.
This thesis is made of three thematic parts. In the first part a review on the ecology
and evolution of siboglinids worms is presented. Four siboglinids groups are known; Vesti-
mentifera, Monolifera (Sclerolinum), Frenulata and Osedax. All siboglinids lack a mouth,
gut and anus and rely on symbiotic bacteria for their nutrition. Siboliginid symbionts
include different lineages of sulfur-oxidising and methane-oxidising Gammaproteobacteria,
and heterotrophic Oceanospirillales bacteria. Siboglinids occur in a various range of re-
duced habitats: from organic rich sediment, to whale falls, vents and seeps. The diversity
of their symbionts and the variety of habitats where they occur, have strongly influenced
their ecology and their evolution. This review proposes several scenarios addressing how
and when siboglinid ancestors, probably heterotrophic polychaetes, became obligate en-
dosymbiotic species.
The second part focuses on the diversity of the symbionts associated with Osedax mu-
cofloris, at shallow whale falls in the North Atlantic. Before this study, endosymbionts have
been characterised in only five Osedax species from the Pacific Ocean. A high intraspe-
cific symbiont diversity was found in each host species, which was associated with several
bacterial groups within the Oceanospirillales bacteria. In O. mucofloris a higher diversity
of Oceanospirillales bacteria was identified with eight monophyletic clusters and with con-
siderable microheterogeneity within clusters. The symbiont clusters were not uniformly
distributed, but one cluster dominated the population and each individual. In addition,
9when several clusters co-occurred in one individual they were not mixed but were spatially
separated. Multivariate statistical analyses showed that each O. mucofloris individual has
a significant effect on symbionts diversity and distribution. Thus, each O. mucofloris in-
dividual has its own specific endosymbiont community. Our results suggest a horizontal
transmission of the symbionts. Several scenarios explaining the observed symbionts distri-
bution are considered including a flexible selection by the host, variability of the available
symbionts in the environment, and competition between the symbionts.
The third part of this thesis focuses on the symbionts of another polycheate worm, a
Ctenodrilidae, Raricirrus beryli. Bacteria associated with R. beryli gut and worm surface
were highly diverse, belonging to several phyla, including Gammaproteobacteria, Epsilon-
proteobacteria, Firmicutes and Bacteroidetes. Furthermore, among the epibacteria, bac-
teria forming a monophyletic cluster with thiotrophic symbionts of bathymodiolin mussels
were found. This is the first report of a polychaete host for these bacteria. It shows their
ubiquit