On giant shoulders: how a seamount affects the microbial community composition of seawater and sponges

Abstract

<jats:p>Abstract. Seamounts represent ideal systems to study the influence and interdependency of environmental gradients at a single geographic location. These topographic features represent a prominent habitat for various forms of life, including microbiota and macrobiota, spanning benthic as well as pelagic organisms. While it is known that seamounts are globally abundant structures, it still remains unclear how and to which extent the complexity of the sea floor is intertwined with the local oceanographic mosaic, biogeochemistry, and microbiology of a seamount ecosystem. Along these lines, the present study aimed to explore whether and to what extent seamounts can have an imprint on the microbial community composition of seawater and of sessile benthic invertebrates, sponges. For our high-resolution sampling approach of microbial diversity (16S rRNA gene amplicon sequencing) along with measurements of inorganic nutrients and other biogeochemical parameters, we focused on the Schulz Bank seamount ecosystem, a sponge ground ecosystem which is located on the Arctic Mid-Ocean Ridge. Seawater samples were collected at two sampling depths (mid-water, MW, and near-bed water, BW) from a total of 19 sampling sites. With a clustering approach we defined microbial microhabitats within the pelagic realm at Schulz Bank, which were mapped onto the seamount's topography and related to various environmental parameters (such as suspended particulate matter, SPM; dissolved inorganic carbon, DIC; silicate, SiO4-; phosphate, PO43-; ammonia, NH4+; nitrate, NO32-; nitrite, NO2-; depth; and dissolved oxygen, O2). The results of our study reveal a “seamount effect” (sensu stricto) on the microbial mid-water pelagic community at least 200 m above the sea floor. Further, we observed a strong spatial heterogeneity in the pelagic microbial landscape across the seamount, with planktonic microbial communities reflecting oscillatory and circulatory water movements, as well as processes of bentho-pelagic coupling. Depth, NO32-, SiO4-, and O2 concentrations differed significantly between the determined pelagic microbial clusters close to the sea floor (BW), suggesting that these parameters were presumably linked to changes in microbial community structures. Secondly, we assessed the associated microbial community compositions of three sponge species along a depth gradient of the seamount. While sponge-associated microbial communities were found to be mainly species-specific, we also detected significant intra-specific differences between individuals, depending on the pelagic near-bed cluster they originated from. The variable microbial phyla (i.e. phyla which showed significant differences across varying depth, NO32-, SiO4-, O2 concentrations, and different from local seawater communities) were distinct for every sponge species when considering average abundances per species. Variable microbial phyla included representatives of both those taxa traditionally counted for the variable community fraction and taxa counted traditionally for the core community fraction. Microbial co-occurrence patterns for the three examined sponge species Geodia hentscheli, Lissodendoryx complicata, and Schaudinnia rosea were distinct from each other. Over all, this study shows that topographic structures such as the Schulz Bank seamount can have an imprint (seamount effect sensu lato) on both the microbial community composition of seawater and sessile benthic invertebrates such as sponges by an interplay between the geology, physical oceanography, biogeochemistry, and microbiology of seamounts. </jats:p>

Seasonal Variability in Near-bed Environmental Conditions in the Vazella pourtalesii Glass Sponge Grounds of the Scotian Shelf

“…Atlantic (Rice et al, 1990) or the Faroe Shetland channel where sponges were observed in regions with intensified internal wave activity and associated with pronounced changes in temperature (Davison et al, 2019). Such conditions have also been found on seamounts and canyons, where sponge aggregations have been observed in areas of critical slope in the Arctic (Schulz Bank seamount; Busch et al, 2020) and the Azores (Rainbow Basin;van Haren et al, 2017). Based on our data we can only link the environmental fluctuations to the presence of tidal currents.…”

“…Water column mixing will result in an increased availability of nutrients from the deeper water masses toward the surface (Townsend et al, 2006), triggering primary productivity and increased benthic-pelagic coupling (Ji et al, 2006). Topography-hydrography interactions can also influence biogeochemistry and microbiology either by mixing or by resuspension as described above, which can result in different sponge associated microbial communities defined by the surrounding near-bed environment (Busch et al, 2020). This mixing will indirectly promote an increased vertical flux and therefore food supply to the sponge grounds and their associated fauna, as was also observed in the Gulf of Mexico and on the Namibian margin (Mienis et al, 2012;Hanz et al, 2019).…”

Bacterial precursors and unsaturated long-chain fatty acids are biomarkers of North-Atlantic deep-sea demosponges

“…A proposed candidate phylum for MBFAs is Poribacteria, a unique and abundant phylum in HMA sponges [46], since a positive relation between MBFA concentration and Poribacteria abundance was found across several sponge species [44]. Metagenome analyses showed that Poribacteria are a prominent phylum in G. barretti [47,48], but are rare or even absent in G. hentscheli [49], which shows a dominance of Acidobacteria, Chloroflexi, and Proteobacteria, phyla that are also abundant in G. barretti [47,48]. This suggests that either the MBFAs belong to one of the above-mentioned phyla, or that the MBFAs are shared among microbial phyla, as their chemotaxonomic resolution is lower compared to genomic analysis.…”

A Microbial Nitrogen Engine Modulated by Bacteriosyncytia in Hexactinellid Sponges: Ecological Implications for Deep-Sea Communities

“…In order to examine the microbial diversity in the studied sponges, 13 individuals of V. pourtalesii were collected from Sambro Bank and 13 of S. rosea from Schulz Bank. The sample processing procedure is described in detail elsewhere (Busch et al, 2020(Busch et al, , 2021; see also these references for data availability). Briefly, from each sponge individual chunks of tissue were subsampled, rinsed and frozen at −80 • C until DNA extraction.…”