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Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium

View ORCID ProfileYui Sato, Juliane Wippler, Cecilia Wentrup, View ORCID ProfileRebecca Ansorge, Miriam Sadowski, View ORCID ProfileHarald Gruber-Vodicka, View ORCID ProfileNicole Dubilier, View ORCID ProfileManuel Kleiner
doi: https://doi.org/10.1101/2021.01.30.428904
Yui Sato
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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  • For correspondence: ysato@mpi-bremen.de ndubilie@mpi-bremen.de manuel_kleiner@ncsu.edu
Juliane Wippler
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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Cecilia Wentrup
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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Rebecca Ansorge
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
2Quadram Institute Bioscience, Gut Microbes and Health Programme, Norwich NR4 7UQ, UK
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Miriam Sadowski
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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Harald Gruber-Vodicka
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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Nicole Dubilier
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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  • For correspondence: ysato@mpi-bremen.de ndubilie@mpi-bremen.de manuel_kleiner@ncsu.edu
Manuel Kleiner
3North Carolina State University, Department of Plant and Microbial Biology, Raleigh, North Carolina 27695, USA
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  • ORCID record for Manuel Kleiner
  • For correspondence: ysato@mpi-bremen.de ndubilie@mpi-bremen.de manuel_kleiner@ncsu.edu
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Abstract

In obligate symbioses, partner fidelity plays a central role in maintaining the association over evolutionary time. Fidelity has been well studied in hosts with only a few symbionts, but little is known about how fidelity is maintained in obligate associations with multiple co-occurring symbionts. Here, we show that partner fidelity varies from strict to absent in a gutless marine annelid and its consortium of co-occurring symbionts that provide it with nutrition. We sequenced the metagenomes of 80 Olavius algarvensis individuals from the Mediterranean, and compared host mitochondrial and symbiont phylogenies based on single nucleotide polymorphisms across genomes, using a low-coverage sequencing approach that has not yet been applied to microbial community analyses. Fidelity was strongest for the two chemoautotrophic, sulphur-oxidizing symbionts that dominated the microbial consortium in all host individuals. In contrast, fidelity was only intermediate to absent in the sulphate-reducing and spirochaetal symbionts, which occurred in lower abundance and were not always present in all host individuals. We propose that variable degrees of fidelity are advantageous for these hosts by allowing the faithful transmission of their nutritionally most important symbionts and flexibility in the acquisition of other symbionts that promote ecological plasticity in the acquisition of environmental resources.

Competing Interest Statement

The authors have declared no competing interest.

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Posted November 24, 2021.
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Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium
Yui Sato, Juliane Wippler, Cecilia Wentrup, Rebecca Ansorge, Miriam Sadowski, Harald Gruber-Vodicka, Nicole Dubilier, Manuel Kleiner
bioRxiv 2021.01.30.428904; doi: https://doi.org/10.1101/2021.01.30.428904
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Fidelity varies in the symbiosis between a gutless marine worm and its microbial consortium
Yui Sato, Juliane Wippler, Cecilia Wentrup, Rebecca Ansorge, Miriam Sadowski, Harald Gruber-Vodicka, Nicole Dubilier, Manuel Kleiner
bioRxiv 2021.01.30.428904; doi: https://doi.org/10.1101/2021.01.30.428904

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