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Sponge-derived matter is assimilated by coral holobionts.

ABSTRACT: Coral reef biodiversity is maintained by a complex network of nutrient recycling among organisms. Sponges assimilate nutrients produced by other organisms like coral and algae, releasing them as particulate and dissolved matter, but to date, only a single trophic link between sponge-derived dissolved matter and a macroalgae has been identified. We sought to determine if sponge-coral nutrient exchange is reciprocal using a stable isotope 'pulse-chase' experiment to trace the uptake of ¹³C and ¹⁵N sponge-derived matter by the coral holobiont for three coral species (Acropora cervicornis, Orbicella faveolata, and Eunicea flexuosa). Coral holobionts incorporated 2.3-26.8x more ¹⁵N than ¹³C from sponge-derived matter and A. cervicornis incorporated more of both C and N than the other corals. Differential isotopic incorporation among coral species aligns with their ecophysiological characteristics (e.g., morphology, Symbiodiniaceae density). Our results elucidate a recycling pathway on coral reefs that has implications for improving coral aquaculture and management approaches.

SUBMITTER: Reigel AM

PROVIDER: S-EPMC10837432 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Sponge-derived matter is assimilated by coral holobionts.

Reigel Alicia M AM Easson Cole G CG Apprill Amy A Freeman Christopher J CJ Bartley Michaela M MM Fiore Cara L CL

Communications biology 20240202 1

Coral reef biodiversity is maintained by a complex network of nutrient recycling among organisms. Sponges assimilate nutrients produced by other organisms like coral and algae, releasing them as particulate and dissolved matter, but to date, only a single trophic link between sponge-derived dissolved matter and a macroalgae has been identified. We sought to determine if sponge-coral nutrient exchange is reciprocal using a stable isotope 'pulse-chase' experiment to trace the uptake of <sup>13</su ...[more]

PMID: 38308082

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Project description:BackgroundSponge holobionts (i.e., the host and its associated microbiota) play a key role in the cycling of dissolved organic matter (DOM) in marine ecosystems. On coral reefs, an ecological shift from coral-dominated to algal-dominated ecosystems is currently occurring. Given that benthic corals and macroalgae release different types of DOM, in different abundances and with different bioavailability to sponge holobionts, it is important to understand how the metabolic activity of the host and associated microbiota change in response to the exposure to both DOM sources. Here, we look at the differential gene expression of two sponge holobionts 6 hours after feeding on naturally sourced coral- and macroalgal-DOM using RNA sequencing and meta-transcriptomic analysis.ResultsWe found a slight, but significant differential gene expression in the comparison between the coral- and macroalgal-DOM treatments in both the high microbial abundance sponge Plakortis angulospiculatus and the low microbial abundance sponge Haliclona vansoesti. In the hosts, processes that regulate immune response, signal transduction, and metabolic pathways related to cell proliferation were elicited. In the associated microbiota carbohydrate metabolism was upregulated in both treatments, but coral-DOM induced further lipid and amino acids biosynthesis, while macroalgal-DOM caused a stress response. These differences could be driven by the presence of distinct organic macronutrients in the two DOM sources and of small pathogens or bacterial virulence factors in the macroalgal-DOM.ConclusionsThis work provides two new sponge meta-transcriptomes and a database of putative genes and genetic pathways that are involved in the differential processing of coral- versus macroalgal-DOM as food source to sponges with high and low abundances of associated microbes. These pathways include carbohydrate metabolism, signaling pathways, and immune responses. However, the differences in the meta-transcriptomic responses of the sponge holobionts after 6 hours of feeding on the two DOM sources were small. Longer-term responses to both DOM sources should be assessed to evaluate how the metabolism and the ecological function of sponges will be affected when reefs shift from coral towards algal dominance.

Project description:The microbial communities associated with sponges contribute to the adaptation of hosts to environments, which are essential for the trophic transformation of benthic-marine coupling. However, little is known about the symbiotic microbial community interactions and adaptative strategies of high- and low-microbial abundance (HMA and LMA) sponges, which represent two typical ecological phenotypes. Here, we compared the 1-year dynamic patterns of microbiomes with the HMA sponge Spongia officinalis and two LMA sponge species Tedania sp. and Haliclona simulans widespread on the coast of China. Symbiotic bacterial communities with the characteristic HMA-LMA dichotomy presented higher diversity and stability in S. officinalis than in Tedania sp. and H. simulans, while archaeal communities showed consistent diversity across all sponges throughout the year. Dissolved oxygen, dissolved inorganic phosphorus, dissolved organic phosphorus, and especially temperature were the major factors affecting the seasonal changes in sponge microbial communities. S. officinalis-associated microbiome had higher diversity, stronger stability, and closer interaction, which adopted a relatively isolated strategy to cope with environmental changes, while Tedania sp. and H. simulans were more susceptible and shared more bacterial Amplicon Sequence Variants (ASVs) with surrounding waters, with an open way facing the uncertainty of the environment. Meta-analysis of the microbiome in composition, diversity, and ecological function from 13 marine sponges further supported that bacterial communities associated with HMA and LMA sponges have evolved two distinct environmental adaptation strategies. We propose that the different adaptive ways of sponges responding to the environment may be responsible for their successful evolution and their competence in global ocean change.ImportanceDuring long-term evolution, sponge holobionts, among the oldest symbiotic relationships between microbes and metazoans, developed two distinct phenotypes with high- and low-microbial abundance (HMA and LMA). Despite sporadic studies indicating that the characteristic microbial assemblages present in HMA and LMA sponges, the adaptation strategies of symbionts responding to environments are still unclear. This deficiency limits our understanding of the selection of symbionts and the ecological functions during the evolutionary history and the adaptative assessment of HMA and LMA sponges in variable environments. Here, we explored symbiotic communities with two distinct phenotypes in a 1-year dynamic environment and combined with the meta-analysis of 13 sponges. The different strategies of symbionts in adapting to the environment were basically drawn: microbes with LMA were more acclimated to environmental changes, forming relatively loose-connected communities, while HMA developed relatively tight-connected and more similar communities beyond the divergence of species and geographical location.

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Sponge-derived matter is assimilated by coral holobionts.

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Sponge-derived matter is assimilated by coral holobionts.

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