Success of chemolithoautotrophic SUP05 and Sulfurimonas GD17 cells in pelagic Baltic Sea redox zones is facilitated by their lifestyles as K‐ and r‐strategists

Abstract

Chemolithoautotrophic sulfur-oxidizing and denitrifying Gamma- (particularly the SUP05 cluster) and Epsilonproteobacteria (predominantly Sulfurimonas subgroup GD17) are assumed to compete for substrates (electron donors and acceptors) in marine pelagic redox gradients. To elucidate their ecological niche separation we performed S , NO3- and H CO3- stable-isotope incubations with water samples from Baltic Sea suboxic, chemocline and sulfidic zones followed by combined phylogenetic staining and high-resolution secondary ion mass spectrometry of single cells. SUP05 cells were small-sized (0.06-0.09 µm ) and most abundant in low-sulfidic to suboxic zones, whereas Sulfurimonas GD17 cells were significantly larger (0.26-0.61 µm ) and most abundant at the chemocline and below. Together, SUP05 and GD17 cells accumulated up to 48% of the labelled substrates but calculation of cell volume-specific rates revealed that GD17 cells incorporated labelled substrates significantly faster throughout the redox zone, thereby potentially outcompeting SUP05 especially at high substrate concentrations. Thus, in synopsis with earlier described features of SUP05/GD17 we conclude that their spatially overlapping association in stratified sulfidic zones is facilitated by their different lifestyles: whereas SUP05 cells are streamlined, non-motile K-strategists adapted to low substrate concentrations, GD17 cells are motile r-strategists well adapted to fluctuating substrate and redox conditions.

A metatranscriptomics‐based assessment of small‐scale mixing of sulfidic and oxic waters on redoxcline prokaryotic communities

“…The pronounced, temporally complementary response to experimental manipulation of taxa affiliated with either Sulfurimonas or SUP05 support the existence of different niches occupied by the respective strains of these chemolithoauthotrophic organisms (Rogge et al ., ). The apparently higher oxygen tolerance of the SUP05 denitrification system may explain the spatial distribution of SUP05 and Sulfurimonas in the Baltic Sea redoxcline, where SUP05 members typically dominate over Sulfurimonas sp.…”

“…The apparently higher oxygen tolerance of the SUP05 denitrification system may explain the spatial distribution of SUP05 and Sulfurimonas in the Baltic Sea redoxcline, where SUP05 members typically dominate over Sulfurimonas sp. in the upper redoxcline while the opposite case is true in lower sulfidic redoxcline zones (Rogge et al ., ). Also the recently reported temporal shift from Sulfurominas to gammaproteobacterial sulfur oxidizer populations in the Cariaco Basin (Taylor et al ., ) could have been linked to such a niche differentiation in response to changing redox levels.…”

Microbial metabolite fluxes in a model marine anoxic ecosystem

“…Given that sulfide oxidation spatially overlaps substantially with nitrate consumption (Fig. 4C), it is probable that nitrate is at least partly used as a terminal electron acceptor for the oxidation of various sulfur compounds, a process observed in other oxygen-depleted regions of the ocean (Canfield et al, 2010;Schunck et al, 2013;Louca et al, 2016;Rogge et al, 2017). Indeed, the Gammaproteobacterial clades BS-GSO2 and SUP05, members of which are frequently implicated in sulfide oxidation and denitrification in oxygen-poor marine systems (Lavik et al, 2009;Walsh et al, 2009;Fuchsman et al, 2012;Glaubitz et al, 2013;Shah et al, 2017;Rogge et al, 2017), have been observed at high relative abundances in the Cariaco Basin redoxcline (Rodriguez-Mora et al, 2015;Taylor et al, 2018;Suter et al, 2018).…”

Microbial metabolite fluxes in a model marine anoxic ecosystem

“…Given that sulfide oxidation spatially overlaps substantially with nitrate consumption (Figure 4c), it is probable that nitrate is at least partly used as a terminal electron acceptor for the oxidation of various sulfur compounds, a process observed in other oxygen-depleted regions of the ocean (Canfield et al, 2010;Louca et al, 2016;Rogge et al, 2017;Schunck et al, 2013). Indeed, the Gammaproteobacterial clades BS-GSO2 and SUP05, members of which are frequently implicated in sulfide oxidation and denitrification in oxygen-poor marine systems (Fuchsman, Murray, & Staley, 2012;Glaubitz, Kießlich, Meeske, Labrenz, & Jürgens, 2013;Lavik et al, 2009;Rogge et al, 2017;Shah, Chang, & Morris, 2017;Walsh et al, 2009), have been observed at high relative abundances in the Cariaco Basin redoxcline respectively. This pattern has been previously partly attributed to a "metal redox shuttle," whereby phosphate is scavenged during ferrous and manganese oxide formation in the redoxcline and subsequently redissolved at depth (Dellwig et al, 2010;McParland et al, 2015;Muller-Karger et al, 2019).…”