Temporal shifts in dominant sulfur-oxidizing chemoautotrophic populations across the Cariaco Basin's redoxcline

Abstract

A pronounced and relatively stable peak in dark carbon assimilation (DCA) has been observed within the Cariaco Basin's redoxcline over a 19-year observation period, presumably driven largely by sulfur-oxidizing chemoautotrophic bacteria (thioautotrophs). As documented in previous reports, this midwater productivity hotspot is associated with prominent biomass peaks, consisting of prokaryoplankton (Bacteria + Archaea) protists and viruses. Early in the time-series, phylogenetic studies (small subunit ribosomal RNA gene libraries) and fluorescent in situ hybridization (FISH) surveys documented that the chemoautotrophic layer was overwhelmingly populated by ε-proteobacteria related to sulfur-oxidizing symbionts from hydrothermal vent systems and β-proteobacteria. However, after May 2009, β- and ε-proteobacteria were no longer detected in significant numbers by FISH or by more exhaustive sequencing efforts (454 pyrosequencing and MiSeq iTag libraries). Sulfur oxidation gene quantification (qPCR) also confirmed that ε-proteobacteria were rare in samples collected after mid-2009 and that the chemoautotrophic layer became dominated by γ-proteobacterial sulfur-oxidizers (GSOs). Monthly hydrographic and chemical data from the CARIACO Ocean Time-Series were examined for temporal changes that might have driven this shift in the dominant thioautotrophs. Within the redoxcline (250–450 m), significant shifts occurred in water density structure and distributions of H2S, NH4+, O2, and NO2- between the β-/ε-proteobacteria-dominated and the γ-proteobacteria-dominated periods. Contrary to observations in other euxinic systems, GSO seem to have a selective advantage over other sulfur-oxidizing lieages during periods of higher and less variable H2S vertical fluxes and higher relative fluxes of H2S to O2 and NO3-. How exactly this changing seascape might have selected for one lineage over another cannot be directly determined. However, spatiotemporal variations in water density and concentration gradients altered vertical fluxes of the major reductant (H2S) and oxidants (O2, NO3-,NO2-), which we postulate provided a more geochemically stable environment favoring GSOs.