Fluid flow stimulates chemoautotrophy in hydrothermally influenced coastal sediments

Abstract

Hydrothermalism in coastal sediments strongly impacts biogeochemical processes and supports chemoautotrophy. Yet, the effect of fluid flow on microbial community composition and rates of chemoautotrophic production is unknown because rate measurements under natural conditions are difficult, impeding an assessment of the importance of these systems. Here, in situ incubations controlling fluid flow along a transect of three geochemically distinct locations at a shallow-water hydrothermal system off Milos (Greece) show that Campylobacteria dominated chemoautotrophy in the presence of fluid flow. Based on injected 13C-labelled dissolved inorganic carbon and its incorporation into fatty acids, we constrained carbon fixation to be as high as 12 µmol C cm−3 d−1, corresponding to areal rates up to 10-times higher than previously reported for coastal sediments, and showed the importance of fluid flow for supplying the necessary substrates to support chemoautotrophy. Without flow, rates were substantially lower and microbial community composition markedly shifted. Our results highlight the importance of fluid flow in shaping the composition and activity of microbial communities of shallow-water hydrothermal vents, identifying them as hotspots of microbial productivity.

Structure and metabolic potential of the prokaryotic communities from the hydrothermal system of Paleochori Bay, Milos, Greece

“…The genus Thiomiscrospira, and the strain Thiomicrospira sp. Milos-T1 isolated at Milos, has been suggested to be a major actor of sulfur oxidation in Paleochori Bay (Brinkhoff et al, 1999), but these results were not supported in a recent study (Sievert et al, 2022(Sievert et al, ), 10.3389/fmicb.2022 Frontiers in Microbiology 15 frontiersin.org and in our dataset the family Thiomicrospiraceae is mainly present only in the yellow patch composition. Similarly, the family of the sulfur oxidizing bacteria Halothiobacillus kellyi isolated at Milos (Sievert et al, 2000b) represents at best 0.9% of any sample.…”

“…In areas of hydrothermal activity, the advective influx of reduced sulfur species can also fuel the growth of sulfur oxidizing organisms (Sievert et al, 2008(Sievert et al, , 2022. At Milos, the fluids contain abundant H 2 S (Fitzsimons et al, 1997), and the sulfidic zone has been shown to reach or nearly reach the seafloor, except directly at the vent where seawater microcirculation allows for oxygen to penetrate a few centimeters (Wenzhöfer et al, 2000;Yücel et al, 2013).…”

“…We find that these mats consist to around 80% of Arcobacteraceae, Sulfurimonadaceae, and Sulfurovaceae, which contain the well-known marine SOB genera Arcobacter, Sulfurimonas, and Sulfurovum, respectively (Wirsen et al, 2002;Inagaki et al, 2003Inagaki et al, , 2004Sievert et al, 2007). In the sediments, the energy densities of sulfide oxidation are very variable, suggesting highly localized processes, but with higher potential for autotrophy in the more hydrothermally influenced areas where sulfide oxidation coupled to the reduction of oxygen, nitrate, and/or nitrite could support much of the chemolithotrophic primary production (Lu et al, 2020;Sievert et al, 2022). As well, sulfur isotopic analyses suggest that H 2 S is oxidized by microbes close to the venting zone (Houghton et al, 2019).…”

“…The bioturbation seafloor type shows all three families, and our ochre patch core seems mostly devoid of Campylobacterota, despite the soxB gene being detected there. Recently, the Sulfurovaceae family was similarly not detected in an in-situ carbon fixation experiment in the mat patches (Sievert et al, 2022). However, community compositions of 0-1 cmbsf hydrothermal and background sediment where Sulfurovaceae is a major part of the composition in both types of sediments have been described (Giovannelli et al, 2013).…”

“…Since, several new microbial species have been isolated from the bay (Jochimsen et al, 1997;Arab et al, 2000;Sievert and Kuever, 2000;Schlesner et al, 2001), while other studies have looked at the microbial communities in general using most probable numbers, denaturing gradient gel electrophoresis, fluorescence in situ hybridization, lipid analysis and 16S rRNA gene clone libraries (Sievert et al, 1999;Giovannelli et al, 2013;Sollich et al, 2017). There are to date only two studies on Paleochori Bay that involve deep-sequencing technology of the 16S rRNA marker gene, both focusing on a single vent (Bühring and Sievert, 2017;Sievert et al, 2022). A detailed structural analysis of the communities throughout Paleochori Bay and their links to patterns of fluid discharge is therefore still missing.…”