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 O₂ ) 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 CH₄ 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.