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.
Bibliografisk noteFunding Information:
Field work at Lough Hyne was carried out with the permission of the National Parks and Wildlife Service of Ireland. This project was funded by Villum Fonden grant no. 16518. A.S. was partly funded by the H2020 Project SponGES (grant agreement no. 679849). We thank Luke Harman and Allen Whittaker of University College Cork. We also thank the Nordcee lab technicians of the Department of Biology at University of Southern Denmark for constant support in the laboratory procedures and Laura Bristow for assistance with CTD data and operation; we give special thanks to Beate Kraft for assistance with resolving and outlining the processes depicted in Fig. 8. In addition, we thank DNASense for the sequencing of the microbial community and the help with the ampvis2 R package, in particular, Rasmus Wollenberg and Kasper Skytte Andersen. We thank two anonymous reviewers for their constructive comments and suggestions, which greatly improved the manuscript. We declare that we have no conflicts of interest.
© 2021 Schuster et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.