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

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. IMPORTANCE The oceans have an uncertain future due to anthropogenic stressors and an uncertain past that is becoming clearer with advances in biogeochemistry. Both past and future oceans were, or will be, deoxygenated in comparison to present conditions. Studying how sponges and their associated microbes tolerate deoxygenation provides insights into future marine ecosystems. Moreover, sponges form the earliest branch of the animal evolutionary tree, and they likely resemble some of the first animals. We determined the effects of variable environmental oxygen concentrations on the microbial communities of several demosponge species during seasonal anoxia in the field. Our results indicate that anoxic tolerance in some sponges may depend on their symbionts, but anoxic tolerance was not universal in sponges. Therefore, some sponge species could likely outcompete benthic organisms like corals in future, reduced-oxygen ecosystems. Our results support the molecular evidence that sponges and other animals have a Neoproterozoic origin and that animal evolution was not limited by low-oxygen conditions.

Adaptive strategies of sponges to deoxygenated oceans

“…Some sponges can live in anoxic conditions for several months, such as the sponges of the family Raspailidae found in the deeper cliffs of Lough Hyne (Bell & Barnes, 2000; McAllen et al, 2009; Micaroni et al, 2021). Schuster et al (2021) suggested that this tolerance could be conferred by specific bacterial symbionts, which are able to carry out anaerobic metabolism. In addition, these sponges living in anoxia are all thin crusts, with a very high surface‐to‐volume ratio, which could favour the exchange of gases and the release of metabolic waste (Levin et al, 1991).…”

“…Species‐specific phenotypic plasticity appears to help these organisms to overcome hypoxic events, and future research will need to elucidate the mechanisms behind these changes. This exceptional adaptive capacity of sponges could be derived from their ancient evolutionary origin and could confer sponges a competitive advantage in future deoxygenated oceans over other organisms (Mills et al, 2014; Schuster et al, 2021).…”

Marine sponges in the once and future ocean

“…Indeed, sponges have diverse and complex microbiomes and are classified as either "highmicrobial-abundance" (HMA) or "low-microbial-abundance" (LMA) based on their bacterial cell densities. As sponges lack essential components of the HIF oxygen-sensing pathway (Mills et al, 2018), it has been suggested that hypoxia and anoxia (zero oxygen) tolerance may be conferred to sponges via metabolic interactions with their microbiome (Schuster et al, 2021). In the laboratory, all sponges analyzed to date-with the exception of G. barretti-are most likely LMA sponges.…”

Metagenomics-resolved genomics provides novel insights into chitin turnover, metabolic specialization, and niche partitioning in the octocoral microbiome

“…One-way permutational analysis of variance (PERMANOVA) was used to test for overall differences in functional profiles among MAGs belonging to different taxonomic orders. To determine COG functions that contributed most to the dissimilarity between MAGs at the order level, similarity percentage analysis (SIMPER) was performed in PAST v 3.25 [84]. The top ten most differentiating COG functions were then plotted as vectors on the PCA diagram to explore relationships between gene functions and symbiont taxonomy.…”