Sargassum Differentially Shapes the Microbiota Composition and Diversity at Coastal Tide Sites and Inland Storage Sites on Caribbean Islands

Abstract

Rafts of drifting pelagic Sargassum that are circulating across the Atlantic Ocean are complex ecosystems composed of a large number of associated species. Upon massive stranding, they lead to various socio-environmental issues including the inflow of contaminants and human health concerns. In this study, we used metabarcoding approaches to examine the differences in both the eukaryotic- and prokaryotic-associated communities from Sargassum present in two islands of the Lesser Antilles, namely Guadeloupe and Martinique. We detected significant differences in microbial community structure and composition between landing Sargassum, the surrounding seawater, and Sargassum from inland storage sites. In total we identified 22,214 prokaryotic and 17,679 eukaryotic OTUs. Among them, functional prediction analyses revealed a number of prokaryotes that might contribute to organic matter decomposition, nitrogen cycling and gas production, including sulfate-reducing bacteria at coastal landing sites, and methanogenic archaea at inland storage sites. We also found that Metazoan was the most abundant group in Sargassum samples, with nematode clades that presented exclusive or specific richness and abundance patterns depending on their Sargassum substrate. Together, these molecular inventories of the micro- and meiofauna communities provide baseline information for further characterization of trophic interactions, algal organic matter decomposition and nutrient transfers at coastal and inland storage sites.

Diversity of the holopelagic Sargassum microbiome from the Great Atlantic Sargassum Belt to coastal stranding locations

“…This is not surprising, since holopelagic Sargassum floats in the marine photic zone and provides an important substrate in open waters for biofilm-producing photosynthetic bacteria. The presence of photosynthetic bacteria agrees with earlier studies on holopelagic Sargassum (Hervé et al, 2021;Michotey et al, 2020;Torralba et al, 2017) and these bacteria could assist in nitrogen fixation as has been shown experimentally (Phlips et al, 1986;Phlips and Zeman, 1990). Samples for microbiome comparison in seawater were not analyzed in this study, however Sargassum samples were washed with 0.2 µm filtered seawater before processing and it thus likely that the described microbiome is associated with Sargassum rather than the neighboring seawater.…”

“…These observations were also reported for the benthic Sargassum muticum (Serebryakova et al, 2018) and Sargassum ilicifolium (Oh et al, 2021). The high abundances of Rhodobacteraceae, Pseudomonadaceae and Vibrionaceae were likely related to the high release of dissolved organic matter (DOM) by holopelagic Sargassum in open waters (Powers et al, 2019;Shank et al, 2010a;Shank et al, 2010b), which stimulates the proliferation of DOM-degrading bacteria in these families of Proteobacteria (Buchan et al, 2014;Hervé et al, 2021).…”

“…These high Vibrio relative abundances were hypothesized as being linked to holopelagic Sargassum growth, resulting in elevated Sargassum exudates that are high in dissolved organic carbon predominantly in open waters rather than stations closer to the shore (Michotey et al, 2020). However, that study considered mostly open water stations rather than coastal stranding locations and there are likely structural differences in the microbiome when holopelagic Sargassum enters coastal waters and forms brown tides (Hervé et al, 2021;Michotey et al, 2020). As macroalgal microbiomes enter dysbiosis, relative abundances of pathogenic opportunistic bacteria may increase in contrast to the microbiome of healthy macroalgae (Minich et al, 2018).…”

“…Torralba et al (2017) indicated that the holopelagic Sargassum microbiome features a diverse microbial community compared to the neighboring seawater, largely composed of photosynthetic and nitrogen-fixing bacteria belonging to the Rhodobacteraceae and Cyanobacteria. Hervé et al (2021) showed that dissolved organic matter (DOM)-degrading bacteria are likely present in groups such as Saprospiraceae and Flavobacteraceae. Furthermore, holopelagic Sargassum genotypes were reported to host similar bacterial OTUs (Operational Taxonomic Units) (Michotey et al, 2020), which is surprising since macroinvertebrate communities may vary between Sargassum genotypes (Govindarajan et al, 2019;Martin et al, 2021).…”

Microbiota changes in a stranding simulation of the holopelagic macroalgae Sargassum natans and Sargassum fluitans

“…One concern related to Sargassum degradation is the production of hydrogen sul de, which is a toxic gas [56], but we have not identi ed any functional group related strickly to the sulfur cycle, indicating that the bacteria associated with such processes are likely found in coastal waters, and not associated with Sargassum from the open ocean. This evidence is supported by Hervé et al (2021)[18] with the identi cation of sulfur-respiring microorganisms in nearshore water samples, as well as in stranded Sargassum.…”