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Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier.

ABSTRACT: Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of phototrophy complementarily according to energy needs and environmental conditions. Here, we report four Tardiphaga sp. strains (Alphaproteobacteria) of monophyletic origin isolated from a high Arctic glacier in northeast Greenland (81.566° N, 16.363° W) that are at different evolutionary stages concerning phototrophy. Their >99.8% identical genomes contain footprints of horizontal operon transfer (HOT) of the complete gene clusters encoding BChl- and xanthorhodopsin (XR)-based dual phototrophy. Two strains possess only a complete XR operon, while the other two strains have both a photosynthesis gene cluster and an XR operon in their genomes. All XR operons are heavily surrounded by mobile genetic elements and are located close to a tRNA gene, strongly signaling that a HOT event of the XR operon has occurred recently. Mining public genome databases and our high Arctic glacial and soil metagenomes revealed that phylogenetically diverse bacteria have the metabolic potential of performing BChl- and rhodopsin-based dual phototrophy. Our data provide new insights on how bacteria cope with the harsh and energy-deficient environment in surface glacier, possibly by maximizing the capability of exploiting solar energy.IMPORTANCE Over the course of evolution for billions of years, bacteria that are capable of light-driven energy production have occupied every corner of surface Earth where sunlight can reach. Only two general biological systems have evolved in bacteria to be capable of net energy conservation via light harvesting: one is based on the pigment of (bacterio-)chlorophyll and the other is based on proton-pumping rhodopsin. There is emerging genomic evidence that these two rather different systems can coexist in a single bacterium to take advantage of their contrasting characteristics in the number of genes involved, biosynthesis cost, ease of expression control, and efficiency of energy production and thus enhance the capability of exploiting solar energy. Our data provide the first clear-cut evidence that such dual phototrophy potentially exists in glacial bacteria. Further public genome mining suggests this understudied dual phototrophic mechanism is possibly more common than our data alone suggested.

SUBMITTER: Zeng Y

PROVIDER: S-EPMC7701988 | biostudies-literature | 2020 Nov

REPOSITORIES: biostudies-literature

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Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier.

Zeng Yonghui Y Chen Xihan X Madsen Anne Mette AM Zervas Athanasios A Nielsen Tue Kjærgaard TK Andrei Adrian-Stefan AS Lund-Hansen Lars Chresten LC Liu Yongqin Y Hansen Lars Hestbjerg LH

mBio 20201124 6

Conserving additional energy from sunlight through bacteriochlorophyll (BChl)-based reaction center or proton-pumping rhodopsin is a highly successful life strategy in environmental bacteria. BChl and rhodopsin-based systems display contrasting characteristics in the size of coding operon, cost of biosynthesis, ease of expression control, and efficiency of energy production. This raises an intriguing question of whether a single bacterium has evolved the ability to perform these two types of pho ...[more]

PMID: 33234687

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Project description:BackgroundArctic snowpack microbial communities are continually subject to dynamic chemical and microbial input from the atmosphere. As such, the factors that contribute to structuring their microbial communities are complex and have yet to be completely resolved. These snowpack communities can be used to evaluate whether they fit niche-based or neutral assembly theories.MethodsWe sampled snow from 22 glacier sites on 7 glaciers across Svalbard in April during the maximum snow accumulation period and prior to the melt period to evaluate the factors that drive snowpack metataxonomy. These snowpacks were seasonal, accumulating in early winter on bare ice and firn and completely melting out in autumn. Using a Bayesian fitting strategy to evaluate Hubbell's Unified Neutral Theory of Biodiversity at multiple sites, we tested for neutrality and defined immigration rates at different taxonomic levels. Bacterial abundance and diversity were measured and the amount of potential ice-nucleating bacteria was calculated. The chemical composition (anions, cations, organic acids) and particulate impurity load (elemental and organic carbon) of the winter and spring snowpack were also characterized. We used these data in addition to geographical information to assess possible niche-based effects on snow microbial communities using multivariate and variable partitioning analysis.ResultsWhile certain taxonomic signals were found to fit the neutral assembly model, clear evidence of niche-based selection was observed at most sites. Inorganic chemistry was not linked directly to diversity, but helped to identify predominant colonization sources and predict microbial abundance, which was tightly linked to sea spray. Organic acids were the most significant predictors of microbial diversity. At low organic acid concentrations, the snow microbial structure represented the seeding community closely, and evolved away from it at higher organic acid concentrations, with concomitant increases in bacterial numbers.ConclusionsThese results indicate that environmental selection plays a significant role in structuring snow microbial communities and that future studies should focus on activity and growth. Video Abstract.

Dataset Information

Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier.

Publications

Potential Rhodopsin- and Bacteriochlorophyll-Based Dual Phototrophy in a High Arctic Glacier.

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