Trophic specialisation of metazoan meiofauna at the Håkon Mosby Mud Volcano: fatty acid biomarker isotope evidence

Abstract

We report the results of a detailed investigation on the trophoecology of two dominant meiofaunal species at the HAyenkon Mosby Mud Volcano (HMMV), a deep-sea cold methane-venting seep. Analyses of fatty acids (FAs) and their stable carbon isotopes were used to determine the importance of chemosynthetic nutritional pathways for the dominant copepod species (morphologically very similar to Tisbe wilsoni) inhabiting the volcano's centre and the abundant nematode Halomonhystera disjuncta from the surrounding microbial mats. The strong dominance of bacterial biomarkers (16:1 omega 7c, 18:1 omega 7c and 16:1 omega 8c) coupled with their individual light carbon isotopes signatures (delta C-13 ranging from -52 to -81aEuro degrees) and the lack of symbiotic relationships with prokaryotes (as revealed by molecular analyses and fluorescent in situ hybridisation) indicated that chemosynthetically derived carbon constitutes the main diet of both species. However, the copepod showed a stronger reliance on the utilisation of methanotrophic bacteria and contained polyunsaturated FAs of bacterial origin (20:5 omega 3 and 22:6 omega 3 with isotope signatures delta C-13 < -80aEuro degrees). Instead, the FA profiles of H. disjuncta suggested that sulphide-oxidising bacteria constituted the main diet of this nematode. Therefore, HMMV can be regarded as a persistent deep-sea cold seep, allowing a chemosynthesis-based trophic specialisation by the dominant meiofaunal species inhabiting its sediments. The present investigation, through the determination of the fatty acid profiles, provides the first evidence for trophic specialisation of meiofauna associated with sub-habitats within a cold seep

Closely related intertidal and deep-sea Halomonhystera species have distinct fatty acid compositions

“…Higher 16:1ω7 proportions in H. hermesi could, therefore, be important in HVA to low temperatures. However, the high 16:1ω7 proportions could also have originated from the deep-sea HMMV bacteria Beggiatoa sp., the proposed food source for H. hermesi which is rich in 16:1ω7 [72]. This MUFA has formerly been reported in Beggiatoa species from other cold seeps [20], suggesting that high 16:1ω7 proportions might be important in HVA to cold-seep environments for Beggiatoa and in extension also for organisms feeding on the bacteria such as H. hermesi.…”

“…We investigated the effect of three abiotic factors salinity, temperature and sulphide on total fatty acid composition. Each of the three abiotic factors varied from control conditions (salinity of 25, 16 °C and no sulphide) to environmental conditions representative of the HMMV (salinity of 34-35, −0.9 °C and hydrogen sulphide concentrations up to 1 mM) [58,72]. As previously mentioned, temperature decrease has a clear effect on the FA composition in cellular membranes resulting in an increase in the unsaturated fatty acid proportions.…”

Microbes, macrofauna, and methane: A novel seep community fueled by aerobic methanotrophy

“…40% of the microbial community within a hydrocarbon seep microbial mat at Coal Point (off California) was composed of aerobic methanotrophs, which had the same (n-6) and (n-8) biomarkers observed here (Ding and Valentine 2008). At Hå kon Mosby Mud Volcano (Barents Sea), another welloxygenated seep setting, nematodes consumed aerobic methanotrophic production (Van Gaever et al 2009), yet only 1-3% of methane is oxidized aerobically at this seep site in contrast to 37% of methane being oxidized by anaerobic processes (Niemann et al 2006;Reeburg 2007). In rice paddies, aerobic methanotrophs are preferentially grazed upon by protists (Murase and Frenzel 2007).…”

“…FA profiles of consumers reflect a combination of items incorporated directly from their diets and those synthesized by the consumer along known pathways. Importance of bacterial production or recycling has been demonstrated through FA analysis, and this technique has begun to be employed more extensively to identify the heterotrophic interactions at methane seep ecosystems (MacAvoy et al 2003;Van Gaever et al 2009;Thurber et al 2012).…”

Ecosystem function and services provided by the deep sea

“…Biomasses of methane-consuming bacteria and archaea (3 mol C m −2 ; Boetius and Suess 2004) are directly consumed by a diversity of metazoans (Levin and Michener, 2002;Van Gaever et al, 2009;Levin et al, 2010;Thurber et al, 2012, and the flux of energy out of the benthos, largely in dissolved form (seep fluids can contain ∼ 22 mM of dissolved organic carbon; Valentine et al, 2005), may be an important source of support for deep-sea populations. This results in a vent and seep biomass that far exceeds that of the background community; vents can be found with > 70 kg animal m −2 (Gebruk et al, 2000) and seeps can exceed 30-51 kg animal m −2 (Olu et al, 1996).…”