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Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California.

ABSTRACT: Red-pigmented biofilms grow on rock and cobble surfaces present in anoxic hot springs located on Paoha Island in Mono Lake. The bacterial community was dominated ( approximately 85% of 16S rRNA gene clones) by sequences from the photosynthetic Ectothiorhodospira genus. Scraped biofilm materials incubated under anoxic conditions rapidly oxidized As(III) to As(V) in the light via anoxygenic photosynthesis but could also readily reduce As(V) to As(III) in the dark at comparable rates. Back-labeling experiments with (73)As(V) demonstrated that reduction to (73)As(III) also occurred in the light, thereby illustrating the cooccurrence of these two anaerobic processes as an example of closely coupled arsenotrophy. Oxic biofilms also oxidized As(III) to As(V). Biofilms incubated with [(14)C]acetate oxidized the radiolabel to (14)CO(2) in the light but not the dark, indicating a capacity for photoheterotrophy but not chemoheterotrophy. Anoxic, dark-incubated samples demonstrated As(V) reduction linked to additions of hydrogen or sulfide but not acetate. Chemoautotrophy linked to As(V) as measured by dark fixation of [(14)C]bicarbonate into cell material was stimulated by either H(2) or HS(-). Functional genes for the arsenate respiratory reductase (arrA) and arsenic resistance (arsB) were detected in sequenced amplicons of extracted DNA, with about half of the arrA sequences closely related ( approximately 98% translated amino acid identity) to those from the family Ectothiorhodospiraceae. Surprisingly, no authentic PCR products for arsenite oxidase (aoxB) were obtained, despite observing aerobic arsenite oxidation activity. Collectively, these results demonstrate close linkages of these arsenic redox processes occurring within these biofilms.

SUBMITTER: Hoeft SE

PROVIDER: S-EPMC2901740 | biostudies-literature | 2010 Jul

REPOSITORIES: biostudies-literature

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Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California.

Hoeft Shelley E SE Kulp Thomas R TR Han Sukkyun S Lanoil Brian B Oremland Ronald S RS

Applied and environmental microbiology 20100528 14

Red-pigmented biofilms grow on rock and cobble surfaces present in anoxic hot springs located on Paoha Island in Mono Lake. The bacterial community was dominated ( approximately 85% of 16S rRNA gene clones) by sequences from the photosynthetic Ectothiorhodospira genus. Scraped biofilm materials incubated under anoxic conditions rapidly oxidized As(III) to As(V) in the light via anoxygenic photosynthesis but could also readily reduce As(V) to As(III) in the dark at comparable rates. Back-labeling ...[more]

PMID: 20511421

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Project description:We analyzed the variation with depth in the composition of members of the domain Bacteria in samples from alkaline, hypersaline, and currently meromictic Mono Lake in California. DNA samples were collected from the mixolimnion (2 m), the base of the oxycline (17.5 m), the upper chemocline (23 m), and the monimolimnion (35 m). Composition was assessed by sequencing randomly selected cloned fragments of 16S rRNA genes retrieved from the DNA samples. Most of the 212 sequences retrieved from the samples fell into five major lineages of the domain Bacteria: alpha- and gamma-Proteobacteria (6 and 10%, respectively), Cytophaga-Flexibacter-Bacteroides (19%), high-G+C-content gram-positive organisms (Actinobacteria; 25%), and low-G+C-content gram-positive organisms (Bacillus and Clostridium; 19%). Twelve percent were identified as chloroplasts. The remaining 9% represented beta- and delta-Proteobacteria, Verrucomicrobiales, and candidate divisions. Mixolimnion and oxycline samples had low microbial diversity, with only 9 and 12 distinct phylotypes, respectively, whereas chemocline and monimolimnion samples were more diverse, containing 27 and 25 phylotypes, respectively. The compositions of microbial assemblages from the mixolimnion and oxycline were not significantly different from each other (P = 0.314 and 0.877), but they were significantly different from those of chemocline and monimolimnion assemblages (P < 0.001), and the compositions of chemocline and monimolimnion assemblages were not significantly different from each other (P = 0.006 and 0.124). The populations of sequences retrieved from the mixolimnion and oxycline samples were dominated by sequences related to high-G+C-content gram-positive bacteria (49 and 63%, respectively) distributed in only three distinct phylotypes, while the population of sequences retrieved from the monimolimnion sample was dominated (52%) by sequences related to low-G+C-content gram-positive bacteria distributed in 12 distinct phylotypes. Twelve and 28% of the sequences retrieved from the chemocline sample were also found in the mixolimnion and monimolimnion samples, respectively. None of the sequences retrieved from the monimolimnion sample were found in the mixolimnion or oxycline samples. Elevated diversity in anoxic bottom water samples relative to oxic surface water samples suggests a greater opportunity for niche differentiation in bottom versus surface waters of this lake.

Project description:The Sembawang Hot Spring in Singapore lies at the foot of a major regional geological feature called the Bentong-Raub Suture Zone. Amid an extensively managed surface geothermal park, an undisturbed hot spring emerges with source water at 61°C, pH 6.8, and 1 mg/L dissolved sulfide. A small main pool at the source supported orange-green benthic flocs, whereas the outflow channel with gradually less extreme environmental stress supported extensive vivid green microbial mats. Microscopy revealed that cyanobacterial morphotypes were distinct in flocs and mats at several intervals along the environmental gradient, and we describe a spiraling pattern in the oscillatorian cyanobacteria that may reflect response to poly-extreme stress. Estimation of diversity using 16S rRNA gene sequencing revealed assemblages that were dominated by phototrophic bacteria. The most abundant taxa in flocs at 61°C/1 mg/L sulfide were Roseiflexus sp. and Thermosynechococcus elongatus, whilst the mats at 45.7-55.3°C/0-0.5 mg/L sulfide were dominated by Oscillatoriales cyanobacterium MTP1 and Chloroflexus sp. Occurrence of diverse chemoautotrophs and heterotrophs reflected known thermal ranges for taxa, and of note was the high abundance of thermophilic cellulolytic bacteria that likely reflected the large allochthonous leaf input. A clear shift in ASV-defined putative ecotypes occurred along the environmental stress gradient of the hot spring and overall diversity was inversely correlated to environmental stress. Significant correlations for abiotic variables with observed biotic diversity were identified for temperature, sulfide, and carbonate. A network analysis revealed three putative modules of biotic interactions that also reflected the taxonomic composition at intervals along the environmental gradient. Overall, the data indicated that three distinct microbial communities were supported within a small spatial scale along the poly-extreme environmental gradient. The findings add to the growing inventory of hot spring microbiomes and address an important biogeographic knowledge gap for the region.

Dataset Information

Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California.

Publications

Coupled arsenotrophy in a hot spring photosynthetic biofilm at Mono Lake, California.

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