Stable sponge microbiomes at varied oxygen levels. The effects of environmental oxygen on the microbial community structure in demosponges during seasonal anoxia in a marine lake (Lough Hyne, Ireland)

Globally, climate change is expanding oxygen minimum zones (OMZs), while increased nutrient runoff can deplete 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 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/hypoxia in situ in a semi-enclosed 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, though some symbiont sharing occurred under anoxia. At least three symbiont combinations, all including large populations of Thaumarchaeota OTUs, corresponded with deoxygenation tolerance, and some combinations were shared between distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation.