Free‐living chemoautotrophic and particle‐attached heterotrophic prokaryotes dominate microbial assemblages along a pelagic redox gradient

Abstract

Using the anoxic Cariaco Basin as a natural laboratory, particle association of bacterial and archaeal taxa was assessed by iTag sequencing and qPCR gene assays of samples spanning an oxic-anoxic-euxinic gradient. A total of 10%-12% of all bacterial and archaeal cells were found in the particle-associated (PA) fraction, operationally defined as prokaryotes captured on 2.7 µm membranes. Both redox condition and size fraction segregated bacterial taxa. Archaeal taxa varied according to redox conditions, but were similar between size fractions. Taxa putatively associated with chemoautotrophic sulfur oxidation and nitrification dominated the free-living (FL) fraction throughout the oxycline (< 1-120 µM O ) and upper anoxic layer. Bacteria in the oxycline's PA fraction included taxa known to be aerobic and anaerobic chemoorganotrophs. At shallow anoxic depths, PA taxa were primarily affiliated with anaerobic sulfate ( SO42-)-reducing lineages. PA fractions in the most sulfidic samples were dominated by taxa affiliated with CH oxidizing, fermenting and SO42- reducing lineages. Prevalence of particle-associated SO42--reducing taxa and abundant sulfur-oxidizing taxa in both size fractions across the oxic-anoxic interface is consistent with the cryptic sulfur cycling concept. Bacterial assemblage diversity in the PA fraction always exceeded the FL fraction except in the most oxic samples, whereas Archaeal diversity was not consistently different between size fractions. Our results suggest that these particle-associated and free-living bacterial assemblages are functionally different and that the interplay between particle microhabitats and surrounding geochemical regimes is a strong selective force shaping microbial communities throughout the water column.

Microbial metabolite fluxes in a model marine anoxic ecosystem

“…Most of the sulfide, ammonium, and methane input into the system (i.e., via diffusion or in situ production) can be attributed to diffusion from the bottom boundary (91%, 95%, and 97%, respectively), potentially produced near or in the underlying sediments. Our estimates suggest that some hydrogen sulfide is also produced within the water column (depths ∼600–900 m), consistent with the previous detection of sulfate‐reducing bacteria in sinking particles at anoxic depths (Suter et al, ), although some of the apparent sulfide sources may actually be sulfide diffusing out of the sediments on the basin's side walls. The contribution of in situ sulfide sources to overall sulfide fluxes into the redoxcline is relatively small (∼10%) and has decreased in the latter years, based on the estimated ratio of in situ produced versus in situ consumed sulfide.…”

“…Given that sulfide oxidation spatially overlaps substantially with nitrate consumption (Figure c), 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, ; Louca et al, ; Rogge et al, ; Schunck et al, ). 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, ; Glaubitz, Kießlich, Meeske, Labrenz, & Jürgens, ; Lavik et al, ; Rogge et al, ; Shah, Chang, & Morris, ; Walsh et al, ), have been observed at high relative abundances in the Cariaco Basin redoxcline (Rodriguez‐Mora et al, ; Suter et al, ; Taylor et al, ).…”

“…These data revealed the existence of a strong dynamic redox gradient over depth, along which upward diffusing reductants such as hydrogen sulfide are directly or indirectly oxidized by oxidants such as oxygen in a transition zone roughly spanning depths 200–400 m, sometimes referred to as “redoxcline” (Ho et al, ; Li, Taylor, Astor, Varela, & Scranton, ; Taylor et al, ). Concurrent molecular surveys revealed unique microbial communities that exhibit a clear spatial organization across depth, and elevated population densities within the redoxcline (Cernadas‐Martín, Suter, Scranton, Astor, & Taylor, ; Rodriguez‐Mora, Scranton, Taylor, & Chistoserdov, ; Suter, Pachiadaki, Taylor, Astor, & Edgcomb, ; Taylor et al, , ). However, chemical fluxes across space and microbial metabolic rates in Cariaco Basin and other anoxic regions remain poorly quantified and are largely temporally unresolved, thus making a mechanistic connection between chemical transitions and microbial ecological dynamics difficult (Taylor et al, ).…”

Anomalous δ13C in Particulate Organic Carbon at the Chemoautotrophy Maximum in the Cariaco Basin

“…Putative γ‐proteobacteria S‐oxidizers (GSO) dominating the shallow anoxic and euxinic depths were represented by the SUP05 clade and a single OTU in the Ectothiorhodospiraceae family, closely matching an uncultured Thiorhodospira sp. (Suter et al, ). Related GSOs dominate redoxclines of other oxygen‐depleted environments, such as the Black Sea (Fuchsman et al, ), Baltic Sea (Glaubitz et al, ), shelf water on the Namibian coast (Lavik et al, ), Saanich Inlet (Walsh et al, ), and the Pacific Ocean OMZs (Stewart et al, ).…”

“…As in many other stratified oxygen-depleted water columns, chemoautotrophic assemblages across the Cariaco's redox transitional zone are comprised of ammonia-oxidizing, nitrite-oxidizing, anaerobic ammonia-oxidizing (anammox), and reduced sulfur-oxidizing microorganisms (Cernadas-Martin et al, 2017;Montes et al, 2013;Suter et al, 2018;Taylor et al, 2001;Wakeham et al, 2012). During the present study's timeframe (2013)(2014)(2015)(2016)(2017), ammonia-oxidizing archaea in marine group I, ammonia-oxidizing betaand γ-proteobacteria, and nitrite-oxidizing Nitrospina (δ-proteobacteria) have been observed across the oxycline (Cernadas-Martin et al, 2017;Suter et al, 2018).…”