Intermittent Hypoxia and Prolonged Suboxia Measured In situ in a Marine Sponge

Abstract

High Microbial Abundance (HMA) sponges constitute a guild of suspension-feeding sponges that host vast populations of symbiotic microbes. These symbionts mediate a complex series of biogeochemical transformations that fuel the holobiont's metabolism. Although sponges are aerobic animals, suboxic and anaerobic bacteria are known to reside within their bodies. However, little is known about the chemical characteristics of the sponge environment in which they occur and almost no data are available regarding the dissolved oxygen (DO) dynamics inside the holobiont in its natural habitat. In this study we examined the oxygen dynamics in situ in the HMA sponge Theonella swinhoei. A submersed data-logging system equipped with micro-sensors was used to continuously record DO concentrations inside the sponge body and in its outflowing water for up to 48 h. Actively pumping sponges exhibited high DO removal rates punctuated with short bursts of extreme DO uptake (>90 µmol DO L −1 pumped ), never before observed in sponges. Such a high DO removal rate indicates the consumption of a considerable amount of reduced matter, far exceeding the available sources in the surrounding water of the oligotrophic coral-reef ecosystem inhabited by this sponge. The inner body of the sponge remained suboxic throughout the experiments, with short events of further rapid DO concentration decline. Moreover, DO concentrations measured in the body and in the outflowing water were found to be uncorrelated. Our findings support a previous hypothesis of bacterial symbiont farming by the sponge as a potential source for acquiring reduced material. Moreover, this suggests a complex and highly localized control of the holobiont's metabolism, probably associated with the microbial community's metabolism. Our results indicate that temporal micro-environments exist in the sponge at alternating locations, providing suitable conditions for the activity of its anaerobic microbial symbionts.

Osculum dynamics and filtration activity in small single-osculum explants of the demosponge Halichondria panicea

“…The present observed relationship between sponge osculum dynamics and filtration further indicates that asynchronous closure of oscula, as observed in sponges with numerous oscula (Parker 1910, Pfannkuchen et al 2009, may result in a spatially and temporally heterogeneous supply of oxygen (Schläppy et al 2010a, Lavy et al 2016, as well as of food particles.…”

Integrated metabolism in sponge–microbe symbiosis revealed by genome-centered metatranscriptomics

“…Such a coupling is possible if the two processes and their associated population are temporally and/or spatially separated by variations in oxygen concentration or redox potential, which have been described to occur in sponges (Schläppy et al, 2010;Lavy et al, 2016). The facultative nature of the CcPhy metabolism supports its temporal separation from the aerobic metabolisms CcThau and CcNi, while the observation that CcPhy rarely co-occured with the CcThau and CcNi cells would indicate also a spatial separation of their metabolisms (see Figure 7).…”

A novel Chromatiales bacterium is a potential sulfide oxidizer in multiple orders of marine sponges

“…Sponges are aerobic animals but microaerobic conditions can occur within their bodies for prolonged periods of time (Hoffmann et al ., ). A recent study reports consistent suboxic and anoxic conditions in T. swinhoei (Lavy et al ., ). Moreover, ribosomal protein S3 sequences of Deltaproteobacteria and Clostridia, which are likely to be anaerobes, were abundant (x25 and x9 coverage respectively) (Supporting Information Fig.…”

“…Interestingly, the bacterium was found to be a non‐photosynthetic mixotroph. The addition of heterotrophic capability could be crucial in the oxidized environments that frequently occur in the sponge body throughout the day (Lavy et al ., ). Heterotrophic metabolism could also support these bacteria if they are horizontally transferred between sponges via an oxidized seawater environment.…”

“…Similar to other high microbial abundance (HMA) sponges, T. swinhoei has dense tissue and slow water flow through its body (Yahel et al ., ; Weisz et al ., ). A recent study found that microaerobic conditions occur temporally and spatially within the sponge over long periods of time (Lavy et al ., ).…”