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

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 hentscheli, G. parva, G. atlantica, G. 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 Δ5,9 unsaturation, although also Δ9,19 and (yet undescribed) Δ11,21 unsaturations were identified. G. parva and S. rhaphidiophora each produced distinct LCFAs, while G. atlantica, G. 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.

Reproductive Biology of Geodia Species (Porifera, Tetractinellida) From Boreo-Arctic North-Atlantic Deep-Sea Sponge Grounds

“…In addition, a high percentage of their population participated in reproduction, as also mentioned for G. cydonium (Mercurio et al, 2007). So, despite the scarcity of nutrients in these habitats throughout the year, these species seemed to have a high reproductive effort, that together with their interplay with microbial symbionts (Radax et al, 2012;De Kluijver et al, 2020) could explain the dense aggregations of these species in the sponge grounds. This pattern contrasts to the theory that deep-sea benthos has usually a low reproductive effort due to unfavorable abiotic conditions, such as lack of nutrients (e.g., Thorson, 1950).…”

“…A recent study, not yet peer-reviewed, has showed that bacterial symbionts of Geodia spp. (including G. barretti, G. hentscheli, and G. atlantica), provide the host with precursor lipid building blocks, contributing to the synthesis of sponge unsaturated long-chain fatty acids (De Kluijver et al, 2020). So, the high content in lipid yolk might be related to the presence of high microbial abundance in these species, and it might be the case that by-products of bacterial symbionts within the oocytes contribute to the "autosynthetic" activity of lipid formation.…”