Unexpected Abundance and Diversity of Phototrophs in Mats from Morphologically Variable Microbialites in Great Salt Lake, Utah

Microbial mat communities are associated with extensive (∼700 km ) and morphologically variable carbonate structures, termed microbialites, in the hypersaline Great Salt Lake (GSL), Utah. However, whether the composition of GSL mat communities covaries with microbialite morphology and lake environme...

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Published in:Applied and environmental microbiology 2020-05, Vol.86 (10)
Main Authors: Kanik, Mert, Munro-Ehrlich, Mason, Fernandes-Martins, Maria Clara, Payne, Devon, Gianoulias, Kathryn, Keller, Lisa, Kubacki, Alexander, Lindsay, Melody R, Baxter, Bonnie K, Vanden Berg, Michael D, Colman, Daniel R, Boyd, Eric S
Format: Article
Language:English
Subjects:
Abundance
Adaptation
Bacteria
Bacteriochlorophyll
Biosynthesis
Calvin cycle
Energy conservation
Energy harvesting
Energy metabolism
Heterotrophic bacteria
Heterotrophs
Metabolism
Metagenomics
Microbial Ecology
Microbial mats
Microorganisms
Morphology
Niche overlap
Nitrogenase
Populations
Proteins
Rhodopsin
Robustness
Rocks
Salinity
Salinity effects
Salts
Taxa
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Summary:Microbial mat communities are associated with extensive (∼700 km ) and morphologically variable carbonate structures, termed microbialites, in the hypersaline Great Salt Lake (GSL), Utah. However, whether the composition of GSL mat communities covaries with microbialite morphology and lake environment is unknown. Moreover, the potential adaptations that allow the establishment of these extensive mat communities at high salinity (14% to 17% total salts) are poorly understood. To address these questions, microbial mats were sampled from seven locations in the south arm of GSL representing different lake environments and microbialite morphologies. Despite the morphological differences, microbialite-associated mats were taxonomically similar and were dominated by the cyanobacterium and several heterotrophic bacteria. Metagenomic sequencing of a representative mat revealed and subdominant populations that harbor the Calvin cycle and nitrogenase, suggesting they supply fixed carbon and nitrogen to heterotrophic bacteria. Fifteen of the next sixteen most abundant taxa are inferred to be aerobic heterotrophs and, surprisingly, harbor reaction center, rhodopsin, and/or bacteriochlorophyll biosynthesis proteins, suggesting aerobic photoheterotrophic (APH) capabilities. Importantly, proteins involved in APH are enriched in the GSL community relative to that in microbialite mat communities from lower salinity environments. These findings indicate that the ability to integrate light into energy metabolism is a key adaptation allowing for robust mat development in the hypersaline GSL. The earliest evidence of life on Earth is from organosedimentary structures, termed microbialites, preserved in 3.481-billion-year-old (Ga) rocks. Phototrophic microbial mats form in association with an ∼700-km expanse of morphologically diverse microbialites in the hypersaline Great Salt Lake (GSL), Utah. Here, we show taxonomically similar microbial mat communities are associated with morphologically diverse microbialites across the lake. Metagenomic sequencing reveals an abundance and diversity of autotrophic and heterotrophic taxa capable of harvesting light energy to drive metabolism. The unexpected abundance of and diversity in the mechanisms of harvesting light energy observed in GSL mat populations likely function to minimize niche overlap among coinhabiting taxa, provide a mechanism(s) to increase energy yield and osmotic balance during salt stress, and enhance fitness. Together,
ISSN:0099-2240
1098-5336
DOI:10.1128/AEM.00165-20