Demospongiae, Porifera, Thaumarchaeota, anoxia, deoxygenation, hostmicrobe
interactions, microbiome
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
AQ: A varied oxygen conditions, which was further explored for Eurypon sp. strain 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.