Effects of Seasonal Anoxia on theMicrobial Community Structure in Demosponges in a Marine Lake in Lough Hyne, Ireland

Astrid Schuster*, Brian W. Strehlow, Lisa Eckford-Soper, Rob McAllen, Donald E. Canfield

*Corresponding author for this work

Research output: Contribution to journalJournal articleResearchpeer-review

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Abstract

Climate change is expanding marine oxygen minimum zones (OMZs), while anthropogenic nutrient input depletes oxygen concentrations locally. The effects of deoxygenation on animals are generally detrimental; however, some sponges (Porifera) exhibit hypoxic and anoxic tolerance through currently unknown mechanisms. Sponges harbor highly specific microbiomes, which can include microbes with anaerobic capabilities. Sponge-microbe symbioses must also have persisted through multiple anoxic/hypoxic periods throughout Earth’s history. Since sponges lack key components of the hypoxia-inducible factor (HIF) pathway responsible for hypoxic responses in other animals, it was hypothesized that sponge tolerance to deoxygenation may be facilitated by its microbiome. To test this hypothesis, we determined the microbial composition of sponge species tolerating seasonal anoxia and hypoxia in situ in a semienclosed marine lake, using 16S rRNA amplicon sequencing. We discovered a high degree of cryptic diversity among sponge species tolerating seasonal deoxygenation, including at least nine encrusting species of the orders Axinellida and Poecilosclerida. Despite significant changes in microbial community structure in the water, sponge microbiomes were species specific and remarkably stable under varied oxygen conditions, which was further explored for Eurypon spp. 2 and Hymeraphia stellifera. However, some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota, corresponded with deoxygenation tolerance, and some combinations were shared between some distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.

Original languageEnglish
Article numbere00991-20
JournalmSphere
Volume6
Number of pages24
ISSN1535-9786
DOIs
Publication statusPublished - Jan 2021

Bibliographical note

Publisher Copyright:
© 2021 Schuster et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

Keywords

  • anoxia
  • Demospongiae
  • deoxygenation
  • hostmicrobe interactions
  • microbiome
  • Porifera
  • Thaumarchaeota
  • Anaerobiosis
  • Bacteria/classification
  • Bacterial Physiological Phenomena
  • Phylogeny
  • Aquatic Organisms
  • Microbiota/genetics
  • Genetic Variation
  • Lakes/microbiology
  • Animals
  • Climate Change
  • Ireland
  • Porifera/classification
  • Host Microbial Interactions
  • Seasons

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