Microbial Diversity and Putative Diazotrophy in High- and Low-Microbial-Abundance Mediterranean Sponges

Abstract

c Microbial communities associated with marine sponges carry out nutrient transformations essential for benthic-pelagic coupling; however, knowledge about their composition and function is still sparse. We evaluated the richness and diversity of prokaryotic assemblages associated with three high-microbial-abundance (HMA) and three low-microbial-abundance (LMA) sympatric Mediterranean sponges to address their stability and uniqueness. Moreover, to examine functionality and because an imbalance between nitrogen ingestion and excretion has been observed for some of these species, we sequenced nitrogenase genes (nifH) and measured N 2 fixation. The prokaryotic communities in the two sponge types did not differ in terms of richness, but the highest diversity was found in HMA sponges. Moreover, the discrete composition of the communities in the two sponge types relative to that in the surrounding seawater indicated that horizontal transmission and vertical transmission affect the microbiomes associated with the two sponge categories. nifH genes were found in all LMA species and sporadically in one HMA species, and about half of the nifH gene sequences were common between the different sponge species and were also found in the surrounding water, suggesting horizontal transmission.15 N 2 -enriched incubations showed that N 2 fixation was measurable in the water but was not associated with the sponges. Also, the analysis of the isotopic ratio of 15 N to 14 N in sponge tissue indicated that N 2 fixation is not an important source of nitrogen in these Mediterranean sponges. Overall, our results suggest that compositional and functional features differ between the prokaryotic communities associated with HMA and LMA sponges, which may affect sponge ecology. Marine sponges are sessile filter-feeder metazoans that dominate many hard-bottom benthic substrates around the world (1, 2). They filter large volumes of water and efficiently clear particles down to less than 2 m in size (see reference 3 and references therein). Sponges host complex microbial communities that are generally specific, stable, and distinct in composition compared with the characteristics of the microbes in the surrounding seawater (4-7). Their acquisition can be through horizontal transmission from the surrounding water or by vertical transmission, where microbes are transferred from parental sponges to progeny (6,8).Sponge-associated microbes can supply limiting nutrients to the host and process metabolic waste from the host (4, 9, 10), but the rich taxonomy and functional genetic potential of the sponge-associated microbes suggest that they carry out additional functions (11). Sponges have been categorized as those with a high microbial abundance (HMA) and those with a low microbial abundance (LMA) (12), where HMA species harbor dense, diverse microbial communities and LMA species contain fewer and less diverse microorganisms (6,(13)(14)(15). Despite their distinct microbial compositions, HMA and LMA sponges show similar functional gene repertoires, whic...

The Assimilation of Diazotroph-Derived Nitrogen by Scleractinian Corals Depends on Their Metabolic Status

“…Additional 500-ml bottles containing either 450 ml of the mucus mixture or 450 ml of the unfiltered seawater were incubated similarly after adding 50 ml of 15 N 2 -enriched seawater. On the basis of the volume of the incubation bottle and the quantity of 15 N 2 -enriched seawater added, this resulted in a theoretical enrichment of ~9.8 atom% 15 N in the incubation medium of all bottles, similar to previous 15 N 2 studies of corals and sponges (22, 31, 77, 78). The addition of 15 N 2 -enriched seawater can potentially contaminate the sample with trace metals that can affect N 2 fixation rates, particularly in areas were trace metals are limiting (79).…”

Stable isotopes as tracers of trophic interactions in marine mutualistic symbioses

“…For example, 13 C-bicarbonate has been intensively used to follow the assimilation and partitioning of autotrophic and chemosynthetic-acquired carbon in sponges (Freeman, Baker, Easson, & Thacker, 2015), corals (Tremblay, Naumann, Sikorski, Grover, & Ferrier-Pagès, 2012), or deep vent organisms (Riou et al, 2008). Finally, 15 N-N 2 gas was used to show the assimilation of dinitrogen by diazotrophs associated with animals such as sponges and corals (Bednarz et al, 2017;Benavides et al, 2016;Ribes, Dziallas, Coma, & Riemann, 2015), or by the chemosynthetic symbionts of some marine invertebrates (Petersen et al, 2017). Finally, 15 N-N 2 gas was used to show the assimilation of dinitrogen by diazotrophs associated with animals such as sponges and corals (Bednarz et al, 2017;Benavides et al, 2016;Ribes, Dziallas, Coma, & Riemann, 2015), or by the chemosynthetic symbionts of some marine invertebrates (Petersen et al, 2017).…”

Restructuring of the sponge microbiome favors tolerance to ocean acidification

“…a and b). This fact was consistent with previous reports (Schmitt et al ., ; Björk et al ., ; Ribes et al ., ). The ambient water exhibited a higher richness and diversity in the acidified conditions than in the control conditions at the end of the experiment (Welch's test, p = 0.038; Welch's test, p = 0.036; respectively) (Fig.…”

“…To test this hypothesis, we targeted three sympatric sponge species that are abundant and widely distributed in Mediterranean sublittoral rocky‐bottom habitats and that host different microbial diversity: Dysidea avara , with the lowest diversity, Agelas oroides , with intermediate diversity, and Chondrosia reniformis , with the highest diversity (Ribes et al ., ; Erwin et al ., ). We investigated the three sponge species under both current and future acidification conditions as follows: a) the holobiont performance was assessed by measuring growth rate; b) the surface area of the sponge occupied by associated bacteria was measured by CARD‐FISH and confocal microscopy, and c) the microbiome composition was analyzed through 16S rDNA pyrosequencing.…”