Journal article Open Access

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

de Kluijver, Anna; Nierop, Klaas GJ; Morganti, Teresa M; Bart, Martijn C; Slaby, Beate M; Hanz, Ulrike; de Goeij, Jasper M; Mienis, Furu; Middelburg, Jack J

ABSTRACT

Sponges produce distinct fatty acids (FAs) that (potentially) can be used as chemotaxonomic and ecological biomarkers to study endosymbiont-host interactions and the functional ecology of sponges. Here, we present FA profiles of five common habitat-building deep-sea sponges (class Demospongiae, order Tetractinellida), which are classified as high microbial abundance (HMA) species. Geodia hentscheliG. parvaG. atlanticaG. barretti, and Stelletta rhaphidiophora were collected from boreal and Arctic sponge grounds in the North-Atlantic Ocean. Bacterial FAs dominated in all five species and particularly isomeric mixtures of mid-chain branched FAs (MBFAs, 8- and 9-Me-C16:0 and 10 and 11-Me-C18:0) were found in high abundance (together ≥ 20% of total FAs) aside more common bacterial markers. In addition, the sponges produced long-chain linear, mid- and a(i)-branched unsaturated FAs (LCFAs) with a chain length of 24‒28 C atoms and had predominantly the typical Δ5,9unsaturation, although also Δ9,19 and (yet undescribed) Δ11,21 unsaturations were identified. G. parva and S. rhaphidiophora each produced distinct LCFAs, while G. atlanticaG. barretti, and G. hentscheli produced similar LCFAs, but in different ratios. The different bacterial precursors varied in carbon isotopic composition (δ13C), with MBFAs being more enriched compared to other bacterial (linear and a(i)-branched) FAs. We propose biosynthetic pathways for different LCFAs from their bacterial precursors, that are consistent with small isotopic differences found in LCFAs. Indeed, FA profiles of deep-sea sponges can serve as chemotaxonomic markers and support the conception that sponges acquire building blocks from their endosymbiotic bacteria.

ACKNOWLEDGEMENTS We thank Antje Boetius for supporting and promoting this study and organizing the PS101. We thank the captain and crew of PS101 for excellent support at sea. We thank late Hans Tore Rapp (UiB) for organizing the G.O. Sars expeditions and excellent project coordination. We thank Desmond Eefting for analytical assistance. We thank master students Gydo Geijer, Sean Hoetjes, David Lenkes, Floor Wille, and Femke van Dam for their help in the lab and with analyses. We thank Eva de Rijke, Samira Absalah and Stefan Schouten for their help in protocol development. Irene Rijpstra and Volker Thiel are acknowledged for their help with FA identification. We thank Pieter van Rijswijk and Marco Houtekamer for sharing their analytical knowledge and identification libraries. Paco Cardenas is acknowledged for sharing his taxonomic knowledge. AUTHOR CONTRIBUTIONS Conceptualization: Anna de Kluijver. Data curation: Anna de Kluijver. Formal analysis: Anna de Kluijver, Klaas G. J. Nierop, Teresa M. Morganti. Funding acquisition: Jasper M. de Goeij, Furu Mienis, Jack J. Middelburg. Investigation: Anna de Kluijver, Klaas G. J. Nierop, Martijn C. Bart. Methodology: Anna de Kluijver, Klaas G. J. Nierop, Teresa M. Morganti, Jasper M. de Goeij. Resources: Martijn C. Bart, Beate M. Slaby, Ulrike Hanz, Jasper M. de Goeij, Furu Mienis, Jack J. Middelburg. Validation: Anna de Kluijver, Klaas G. J. Nierop. Visualization: Anna de Kluijver. Writing – original draft: Anna de Kluijver. Writing – review & editing: Anna de Kluijver, Klaas G. J. Nierop, Teresa M. Morganti, Mar- tijn C. Bart, Beate M. Slaby, Ulrike Hanz, Jasper M. de Goeij, Furu Mienis, Jack J. Middelburg. SUPPLEMENTARY MATERIAL S1 Fig. Mass spectra of DMDS conducts of C26 (a,b) and C28 (c,d) LCFA with Δ9,19 (a,c) and Δ11,21 (b,d) unsaturation. (PDF) S1 Table. All fatty acid compositional data. This excel file contains fatty acid data (μg g DW- 1 and relative abundance (%), in PL and TL) of individual specimens. The excel file also con- tains the fragments of Me-branched C16 and C18, the relative positions of saturated (branched and linear) FAMEs in hydrogenated samples and the isotope data. (XLSX) DATA AVAILABILITY STATEMENT All relevant data are within the manuscript and its Supporting Information files.
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