Abstract
Past studies of hydrogen cycling in hypersaline microbial mats have shown an active nighttime cycle, with production largely from Cyanobacteria and consumption from sulfate-reducing bacteria (SRB). However, the mechanisms and magnitude of hydrogen cycling have not been extensively studied. Two mats types near Guerrero Negro, Mexico—permanently submerged Microcoleus microbial mat (GN-S), and intertidal Lyngbya microbial mat (GN-I)—were used in microcosm diel manipulation experiments with 3-(3,4-dichlorophenyl)-1,1-dimethylurea (DCMU), molybdate, ammonium addition, and physical disruption to understand the processes responsible for hydrogen cycling between mat microbes. Across microcosms, H2 production occurred under dark anoxic conditions with simultaneous production of a suite of organic acids. H2 production was not significantly affected by inhibition of nitrogen fixation, but rather appears to result from constitutive fermentation of photosynthetic storage products by oxygenic phototrophs. Comparison to accumulated glycogen and to CO2 flux indicated that, in the GN-I mat, fermentation released almost all of the carbon fixed via photosynthesis during the preceding day, primarily as organic acids. Across mats, although oxygenic and anoxygenic phototrophs were detected, cyanobacterial [NiFe]-hydrogenase transcripts predominated. Molybdate inhibition experiments indicated that SRBs from a wide distribution of DsrA phylotypes were responsible for H2 consumption. Incubation with 13C-acetate and NanoSIMS (secondary ion mass-spectrometry) indicated higher uptake in both Chloroflexi and SRBs relative to other filamentous bacteria. These manipulations and diel incubations confirm that Cyanobacteria were the main fermenters in Guerrero Negro mats and that the net flux of nighttime fermentation byproducts (not only hydrogen) was largely regulated by the interplay between Cyanobacteria, SRBs, and Chloroflexi.
Highlights
Hypersaline microbial mats, living analogs of early life on Earth (Des Marais, 2003), are compact and structured laminations of highly diverse microbial communities that undergo significant redox changes over the diel cycle, alternating between oxic and anoxic states
In previous work we showed that nighttime production of hydrogen gas from hypersaline mats of Elkhorn Slough, CA, USA originated within the photic layer of the mats and was primarily attributable to the fermentation activity of Cyanobacteria, especially the dominant filamentous cyanobacterium Microcoleus chthonoplastes, and was largely insensitive to nitrogen fixation (Burow et al, 2012)
In this study, a suite of methods identified that a variety of Cyanobacteria were the dominant fermentive organism responsible for hydrogen production during nighttime constitutive metabolism
Summary
Hypersaline microbial mats, living analogs of early life on Earth (Des Marais, 2003), are compact and structured laminations of highly diverse microbial communities that undergo significant redox changes over the diel (day-night) cycle, alternating between oxic and anoxic states. The metabolic diversity of microbial mats is reflected in a diverse potential for H2 metabolism (Hoehler, 2005), and nitrogen fixation (Omoregie et al, 2004a,b), and previous work has documented significant efflux of H2 from hypersaline microbial mats (Hoehler et al, 2001; Burow et al, 2012) under dark anoxic conditions. These systems are of interest in an ecological frame of reference, and for bioenergy science. Understanding the ecological and environmental factors that control net H2 production is critical to understanding the role of H2 cycling in mat structure and ecology
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