Journal article Open Access

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

Busch, Kathrin; Hanz, Ulrike; Mienis, Furu; Mueller, Benjamin; Franke, Andre; Roberts, Emyr Martyn; Rapp, Hans Tore; Hentschel, Ute

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, PO34; ammonia, NH+4; nitrate, NO2−3; 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, NO2−3, 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, NO2−3, 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.

ACKNOWLEDGEMENTS. This work is dedicated to Hans Tore Rapp, sponge taxonomist, deep-sea explorer, colleague, and friend. Samples included in this study were collected in compliance with the Nagoya Protocol. We thank the crews and scientific parties of RV G. O. Sars cruises GS2016109A, GS2017110, and GS2018108 for great technical support while at sea. We are grateful for sponge sampling by Stig Vågenes and his ROV Ægir 6000 team (UiB), Christine Rooks (UiB) for sampling assistance on board the ship during GS2016109A, and Jasper de Goeij (UvA) for interesting discussions. We further acknowledge Ina Clefsen, Andrea Hethke, Ilona Urbach, and Tonio Hauptmann (Kiel, Germany) for excellent laboratory support with the amplicon pipeline. Corinna Bang (IKMB, Kiel) provided valuable support with the sample sequencing and revised the manuscript before submission. We also thank the two anonymous reviewers for their comments, which helped to improve this paper. FINANCIAL SUPPORT. This research has been supported by the European Union's Horizon 2020 Research and Innovation Programme under grant agreement no. 679849 (the SponGES project). The article processing charges for this open-access publication were covered by a Research Centre of the Helmholtz Association.
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