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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
2University of Vienna, Department of Microbiology and Ecosystem Science, Althanstr. 14, A-1090 Vienna, Austria
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Rebecca Ansorge
1Max Planck Institute for Marine Microbiology, Celsiusstr. 1, D-28359 Bremen, Germany
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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
3Department of Plant and Microbial Biology, North Carolina State University, Raleigh, North Carolina, 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 stability of the association across multiple host generations. Fidelity has been well studied in hosts with a very restricted diversity of symbionts, but little is known about how fidelity is maintained in hosts with multiple co-occurring symbionts. The marine annelid Olavius algarvensis lives in an obligate association with at least five co-occurring bacterial symbionts that are inherited vertically. The symbionts so efficiently supply their hosts with nutrition that these worms have completely reduced their mouth and digestive tract. Here, we investigated partner fidelity in the O. algarvensis symbiosis by sequencing the metagenomes of 80 host individuals from two mitochondrial lineages and two locations in the Mediterranean. Comparative phylogenetic analyses of mitochondrial and symbiont genotypes based on single nucleotide polymorphisms revealed high fidelity for the primary symbiont that dominated the microbial consortium of all 80 O. algarvensis individuals. In contrast, the secondary symbionts of O. algarvensis, which occurred in lower abundance and were not always present in all host individuals, showed only intermediate to low fidelity. We hypothesize that harbouring symbionts with variable levels of fidelity ensures faithful transmission of the most abundant and nutritionally important symbiont, while flexibility in the acquisition of secondary symbionts enhances genetic exchange and retains ecological and evolutionary adaptability.

Competing Interest Statement

The authors have declared no competing interest.

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Posted January 30, 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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