Genomic Insights Into the Lifestyles of Thaumarchaeota Inside Sponges

Markus Haber, Ilia Burgsdorf, Kim M. Handley, Maxim Rubin-Blum, Laura Steindler

Research output: Contribution to journalArticlepeer-review

Abstract

Sponges are among the oldest metazoans and their success is partly due to their abundant and diverse microbial symbionts. They are one of the few animals that have Thaumarchaeota symbionts. Here we compare genomes of 11 Thaumarchaeota sponge symbionts, including three new genomes, to free-living ones. Like their free-living counterparts, sponge-associated Thaumarchaeota can oxidize ammonia, fix carbon, and produce several vitamins. Adaptions to life inside the sponge host include enrichment in transposases, toxin-antitoxin systems and restriction modifications systems, enrichments previously reported also from bacterial sponge symbionts. Most thaumarchaeal sponge symbionts lost the ability to synthesize rhamnose, which likely alters their cell surface and allows them to evade digestion by the host. All but one archaeal sponge symbiont encoded a high-affinity, branched-chain amino acid transporter system that was absent from the analyzed free-living thaumarchaeota suggesting a mixotrophic lifestyle for the sponge symbionts. Most of the other unique features found in sponge-associated Thaumarchaeota, were limited to only a few specific symbionts. These features included the presence of exopolyphosphatases and a glycine cleavage system found in the novel genomes. Thaumarchaeota have thus likely highly specific interactions with their sponge host, which is supported by the limited number of host sponge species to which each of these symbionts is restricted.

Original languageEnglish
Article number622824
JournalFrontiers in Microbiology
Volume11
DOIs
StatePublished - 11 Jan 2021

Bibliographical note

Funding Information:
This study was funded in part by the Gordon and Betty Moore Foundation, through Grant GBMF9352 to LS. MH was supported by an Inter-Institutional fellowship of the University of Haifa and a Helmsley fellowship. MR-B was supported by the Israeli Science Foundation (ISF grant 913/19) and thanks Nicole Dubilier, the Max Planck Institute for

Funding Information:
We acknowledge the University of Chicago Research Computing Center for support in this work and thank the staff of the Inter-University Institute in Eilat, Israel, for their help during this study. Petrosia ficiformis and Theonella swinhoei sponges were collected in compliance with the 2012/38390 and 2013/3839 permits from the Israel Nature and National Parks Protection Authority. We are grateful to the Mexican authorities for granting permission to collect Hymedesmia (Stylopus) methanophila samples (permission of DGOPA: 02540/14 from 5 November 2014) in the southern Gulf of Mexico and thank the MARUM and all individuals who helped during the R/V Meteor research cruise M114. Funding. This study was funded in part by the Gordon and Betty Moore Foundation, through Grant GBMF9352 to LS. MH was supported by an Inter-Institutional fellowship of the University of Haifa and a Helmsley fellowship. MR-B was supported by the Israeli Science Foundation (ISF grant 913/19) and thanks Nicole Dubilier, the Max Planck Institute for Marine Microbiology and the Max Planck Society for further support and funding.

Publisher Copyright:
© Copyright © 2021 Haber, Burgsdorf, Handley, Rubin-Blum and Steindler.

Keywords

  • Hymedesmia (Stylopus) methanophila
  • Petrosia ficiformis
  • Theonella swinhoei
  • archaea
  • sponge (Porifera)
  • symbiosis
  • thaumarchaeota

ASJC Scopus subject areas

  • Microbiology
  • Microbiology (medical)

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