Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses

Abstract

Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65–87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.

Subcellular view of host–microbiome nutrient exchange in sponges: insights into the ecological success of an early metazoan–microbe symbiosis

“…However, compound-specific (e.g. stable isotope) tracer studies have shown that both sponge cells and associated microbes are involved in organic matter assimilation [36,37], and recent nanoscale secondary ion mass spectrometry (NanoSIMS) studies have confirmed that both host choanocytes (sponge filtering cells) and symbionts can directly assimilate DOM [8,38]. It has been hypothesised that microbially assimilated DOM will be translocated to the host [39], while hostprocessed POM will be recycled by microbial symbionts [13], but these metabolic interactions have not yet been tested.…”

Economic valuation of ecosystem services provided by deep-sea sponges

“…Scientific research is advancing in the measurement of nutrient fluxes in several species of sponges. However, sometimes, even if a given flux is measured, the pathway of the uptake and release of a given compound and the involvement of the sponge cells versus its symbiotic organisms can be difficult to discriminate (Rix et al, 2020).…”

“…In a day, a dense sponge ground can efficiently clear all bacteria found in a water column up to 170 m deep . Sponges also consume large quantities of DOM, constituting up to 97 percent of sponge diet (Rix et al, 2020). A recent study has demonstrated that DOM is taken up both by symbiontic bacteria and sponge cells (Rix et al, 2020).…”

Comparative genomics provides insight into the function of broad-host range sponge symbionts

“…Eight of these unique genes encode proteins potentially involved in the transport and metabolism of sugars. Sugar transport/uptake plays an important role in symbiotic interactions [60][61][62][63]. Therefore, the presence of these genes would suggest that sugars are similarly important to the spirochete-sponge interaction.…”