Dataset Information

The Effect of Spring Water Geochemistry on Copper Proteins in Tengchong Hot Springs, China.

ABSTRACT: Copper (Cu) is an essential trace metal cofactor for a variety of proteins; however, excess Cu is toxic to most organisms. Cu homeostasis is maintained by a complex machinery of Cu binding proteins that control the uptake, transport, sequestration, and efflux of Cu ions. Despite the importance of Cu binding proteins in electron transfer, substrate oxidation, superoxide dismutation, and denitrification, little information exists about microbial Cu utilization in extreme environments, where the geochemical conditions may affect Cu bioavailability. Using metagenomic data from 9 hot springs in Tengchong, China, which range in temperature from 42°C to 96°C and in pH from 2.3 to 9, the effects of pH, temperature, and spring geochemistry on the distribution of Cu binding domains of proteins and oxidoreductases were studied. Dissolved Cu and Cu binding domains were detected across all temperature and pH gradients. Cu binding domains of cytochrome c oxidase subunits, heavy-metal-associated domains, and nitrous oxide reductase were detected at all sites. DoxB, a quinol oxidase, and other quinol oxidase subunits were the dominant Cu binding oxidoreductase subunits present at low-pH and high-temperature sites, whereas cbb 3-type cytochrome c oxidase subunits were dominant at high-pH and high-temperature sites. Additionally, aa 3-type cytochrome c oxidase was more prominent than cbb 3-type cytochrome c oxidase under circumneutral-pH conditions. This suggests that the type of cytochrome c oxidase pathway and the Cu proteins employed by microbes to carry out important functions such as energy acquisition and efflux of excess Cu are affected by the physicochemical conditions of the springs.IMPORTANCE Copper is present in a variety of proteins and is required to carry out essential functions by all organisms. However, in hot spring environments, copper availability may be limited due to the high temperatures and the wide range in pH. The significance of our research is in relating the physicochemical environment to the distribution of copper proteins across hot spring environments, which provides increased understanding of primary functions and adaptions in these environments.

SUBMITTER: Srivastava S

PROVIDER: S-EPMC7301866 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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The Effect of Spring Water Geochemistry on Copper Proteins in Tengchong Hot Springs, China.

Srivastava Shreya S Dong Hailiang H Briggs Brandon R BR

Applied and environmental microbiology 20200617 13

Copper (Cu) is an essential trace metal cofactor for a variety of proteins; however, excess Cu is toxic to most organisms. Cu homeostasis is maintained by a complex machinery of Cu binding proteins that control the uptake, transport, sequestration, and efflux of Cu ions. Despite the importance of Cu binding proteins in electron transfer, substrate oxidation, superoxide dismutation, and denitrification, little information exists about microbial Cu utilization in extreme environments, where the ge ...[more]

PMID: 32358007

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Project description:The Rehai and Ruidian geothermal fields, located in Tengchong County, Yunnan Province, China, host a variety of geochemically distinct hot springs. In this study, we report a comprehensive, cultivation-independent census of microbial communities in 37 samples collected from these geothermal fields, encompassing sites ranging in temperature from 55.1 to 93.6°C, in pH from 2.5 to 9.4, and in mineralogy from silicates in Rehai to carbonates in Ruidian. Richness was low in all samples, with 21-123 species-level OTUs detected. The bacterial phylum Aquificae or archaeal phylum Crenarchaeota were dominant in Rehai samples, yet the dominant taxa within those phyla depended on temperature, pH, and geochemistry. Rehai springs with low pH (2.5-2.6), high temperature (85.1-89.1°C), and high sulfur contents favored the crenarchaeal order Sulfolobales, whereas those with low pH (2.6-4.8) and cooler temperature (55.1-64.5°C) favored the Aquificae genus Hydrogenobaculum. Rehai springs with neutral-alkaline pH (7.2-9.4) and high temperature (>80°C) with high concentrations of silica and salt ions (Na, K, and Cl) favored the Aquificae genus Hydrogenobacter and crenarchaeal orders Desulfurococcales and Thermoproteales. Desulfurococcales and Thermoproteales became predominant in springs with pH much higher than the optimum and even the maximum pH known for these orders. Ruidian water samples harbored a single Aquificae genus Hydrogenobacter, whereas microbial communities in Ruidian sediment samples were more diverse at the phylum level and distinctly different from those in Rehai and Ruidian water samples, with a higher abundance of uncultivated lineages, close relatives of the ammonia-oxidizing archaeon "Candidatus Nitrosocaldus yellowstonii", and candidate division O1aA90 and OP1. These differences between Ruidian sediments and Rehai samples were likely caused by temperature, pH, and sediment mineralogy. The results of this study significantly expand the current understanding of the microbiology in Tengchong hot springs and provide a basis for comparison with other geothermal systems around the world.

Project description:We have constructed a conceptual model of biogeochemical cycles and metabolic and microbial community shifts within a hot spring ecosystem via coordinated analysis of the "Bison Pool" (BP) Environmental Genome and a complementary contextual geochemical dataset of ~75 geochemical parameters. 2,321 16S rRNA clones and 470 megabases of environmental sequence data were produced from biofilms at five sites along the outflow of BP, an alkaline hot spring in Sentinel Meadow (Lower Geyser Basin) of Yellowstone National Park. This channel acts as a >22 m gradient of decreasing temperature, increasing dissolved oxygen, and changing availability of biologically important chemical species, such as those containing nitrogen and sulfur. Microbial life at BP transitions from a 92 °C chemotrophic streamer biofilm community in the BP source pool to a 56 °C phototrophic mat community. We improved automated annotation of the BP environmental genomes using BLAST-based Markov clustering. We have also assigned environmental genome sequences to individual microbial community members by complementing traditional homology-based assignment with nucleotide word-usage algorithms, allowing more than 70% of all reads to be assigned to source organisms. This assignment yields high genome coverage in dominant community members, facilitating reconstruction of nearly complete metabolic profiles and in-depth analysis of the relation between geochemical and metabolic changes along the outflow. We show that changes in environmental conditions and energy availability are associated with dramatic shifts in microbial communities and metabolic function. We have also identified an organism constituting a novel phylum in a metabolic "transition" community, located physically between the chemotroph- and phototroph-dominated sites. The complementary analysis of biogeochemical and environmental genomic data from BP has allowed us to build ecosystem-based conceptual models for this hot spring, reconstructing whole metabolic networks in order to illuminate community roles in shaping and responding to geochemical variability.

Dataset Information

The Effect of Spring Water Geochemistry on Copper Proteins in Tengchong Hot Springs, China.

Publications

The Effect of Spring Water Geochemistry on Copper Proteins in Tengchong Hot Springs, China.

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