The effects of seasonal anoxia on the microbial community structure in demosponges in a marine lake (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 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 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, corresponded with deoxygenation tolerance, and some combinations were shared between distantly related hosts. We propose hypothetical host-symbiont interactions following deoxygenation that could confer deoxygenation tolerance.ImportanceThe 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 compared 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).…”

Effects of anthropogenic stressors on temperate mesophotic ecosystems

“…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 derive 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). The symbol < was used when LT50 was not reported, but more than 50% of the organisms died after a certain amount of time; while > was used when LT50 was not reached by the end of the experiment.…”

“…In support of this hypothesis is the encrusting sponges of the family Raspailidae remaining relatively abundant in 2018. These sponges are the only ones abundant in the deeper, periodically anoxic/hypoxic areas of the lough and are better adapted to acidic, hypoxic, H2S-rich conditions (Schuster et al, 2021). While this kind of oceanographic event could occur naturally in systems like Lough Hyne, the nutrient increase recorded at Lough Hyne and the coastal areas of SW Ireland between the 1990s and 2000s could have contributed to the intensification of the anoxic/hypoxic regime as reported in many other areas of the world (Diaz and Rosenberg, 2008).…”

“…Some sponges can live in anoxic conditions for several months, such as the sponges of the family Raspailiidae found in the deeper cliffs of Lough Hyne (Bell and Barnes, 2000;McAllen et al, 2009). 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 release of metabolic waste (Levin et al, 1991).…”