Fermentation couples Chloroflexi and sulfate-reducing bacteria to Cyanobacteria in hypersaline microbial mats

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.

A Post-Genomic View of the Ecophysiology, Catabolism and Biotechnological Relevance of Sulphate-Reducing Prokaryotes

“…Similarly, the photosynthetic mats in the coastal Um Alhool area (Qatar) are subject to dynamic evaporation and characterized by SRRs which correlate with the presence of diverse SRB, including Desulfovibrio, Desulfococcus and Desulfonema phylotypes (Al-Thani et al, 2014). In hypersaline microbial mats from Elkhorn Slough, California and Guerro Negro, Mexico (Lee et al, 2014), a nighttime cycling of hydrogen was recently reported, with H 2 being produced by fermenting cyanobacteria in the dark and consumed by members of the Desulfobacterales. According to single-cell analysis based on 15 N 2 -labelling, N 2 fixation in these mats is performed by the cyanobacterial members (Lyngbya phylotypes) with no apparent contribution from deltaproteobacterial SRB (Woebken et al, 2015).…”

Halophilic microbial communities and their environments

“…Most hydrogenase transcripts were attributed to cyanobacterial [NiFe]-hydrogenases. Chloroflexi and sulfate reducing bacteria are the main consumers of the cyanobacterial fermentation products [36 ]. A study of lipids in a higher-salinity, gypsum-containing mat at Guerrero Negro provided a wealth of biomarkers witnessing the vertical stratification of different prokaryotes [37].…”

Effects of Elevated Carbon Dioxide and Salinity on the Microbial Diversity in Lithifying Microbial Mats

“…This also increases carbonate alkalinity favoring CaCO 3 precipitation. A recent study in hypersaline mats of Guerrero Negro, Mexico, estimated that nearly all the photosynthetically-fixed CO 2 was excreted as fermentation products during nighttime by cyanobacteria and that sulfate reducing bacteria consumed virtually all of this carbon and H 2 [60]. In microbialites, sulfate reduction has been directly correlated to CaCO 3 precipitation and the formation of micritic crusts [15,58].…”