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.

Keywords: Sargassum; epibiont; macroalgae; methanogenic archaea (MA); microbial communities; nematodes; protists; sulfate-reducing bacteria (SRB).

FIGURE 1

Maps of sampled Sargassum tide sites. The year 2018 corresponded to the biggest tide events ever recorded in the Caribbean region. (A) From left to right, the Caribbean Basin, the Guadeloupe archipelago (violet), and the island of Martinique (red). Due to the proximity of the sampled sites, some circles may overlap. (B–E) Photographs of sampling sites. Sargassum accumulated along the shorelines of Guadeloupe at Saint Félix (B), and La Porte d’Enfer (C). In Martinique, Sargassum in the small harbor of Le Marigot city (D), Sargassum pileup at an inland storage site located in the township of Le Diamant (E).

FIGURE 2

Differences in community composition. Both the prokaryotic community (A) and eukaryotic communities (B) presented significant differences (permutation tests for CAP, P < 0.001) between seawater at tide sites (TS-sw, in blue), Sargassum at marine tide sites (TS-sarg, in brown), and Sargassum at inland storage sites (ISS-sarg, in green).

FIGURE 3

Molecular inventory of the biodiversity associated with Sargassum tides from 100 sampled sites. Differences in the observed OTU richness and relative abundance of seawater at tide sites (TS-sw), Sargassum at tide sites (TS-sarg) and inland Sargassum from storage sites (ISS-sarg). (A) Prokaryotic diversity corresponds to 22,214 OTUs obtained from 2,849,100 reads. (B) Eukaryotic diversity corresponds to 17,679 OTUs obtained from 5,326,300 reads.

FIGURE 4

Phylogenetic relationships between the most abundant nematode OTUs associated with Sargassum. The maximum likelihood phylogenetic tree was constructed with PhyML v3.0 using the GTR + G + I model. Branch supports were calculated using a Chi2-based parametric approximate likelihood-ratio test and are represented by black circles for values above 0.90 and gray circles for values between 0.7 and 0.89. OTU sequences are in bold. The horizontal bar plots represent the normalized total abundance of each OTU in the different compartments: TS-sw in blue, TS-sarg in brown, and ISS-sarg in green. Putative trophic groups were assigned following recommendations by Meldal et al. (2007): algivore-omnivore-predator (AOP), bacterivore (B), entomopathogen (E), and vertebrate parasite (VP).

FIGURE 5

Identification of the OTUs presenting significant differential abundance for the different Sargassum-associated samples, via the ANOVA-like differential expression (ALDEx2) analysis. Comparison between tide sites OTUs that are differentially represented between seawater (TS-sw, blue) or Sargassum (TS-sarg, brown): (A) Prokaryotic, and (B) Eukaryotic. Analyses of the Sargassum-associated OTUs that are differentially represented between marine Sargassum (TS-sarg, brown) or terrestrial Sargassum (ISS-sarg, green): (C) Prokaryotic, and (D) Eukaryotic.

FIGURE 6

Heatmap of predicted functions based on the FAPROTAX database. The 22 categories presented here correspond to 2,831 prokaryotic OTUs. Functions were clustered with the weighted pair group method centroid (WPGMC) algorithm based on Euclidean distances. The color scale represents the proportion of each predicted function within a sample.