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

Abstract

Microbial mat communities are associated with extensive (∼700 km2) 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 Euhalothece and several heterotrophic bacteria. Metagenomic sequencing of a representative mat revealed Euhalothece and subdominant Thiohalocapsa 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. IMPORTANCE 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-km2 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, these physiological benefits promote the formation of robust mats that, in turn, influence the formation of morphologically diverse microbialite structures that can be imprinted in the rock record.

Desiccation of ecosystem-critical microbialites in the shrinking Great Salt Lake, Utah (USA)

“…The The community composition of control samples from a microbialite with a healthy periphyton was largely consistent with compositions found at other times and locations [6,16],…”

Salt to conserve: a review on the ecology and preservation of hypersaline ecosystems

“…However, the incorporation of molecular work such as ribosomal RNA (rRNA) gene sequencing and functional genomics to studies on hypersaline biota may help challenge this norm and refine ecological modelling. For example, in Great Salt Lake, the ‘architects’ of microbialite structures have been discerned, namely photosynthetic cyanobacteria and diatoms (Lindsay et al ., 2017, 2019; Kanik et al ., 2020), which echoes that of the Shark Bay stromatolites in Australia (Edgcomb et al ., 2014; Ruvindy et al ., 2016). However, an exploration of the total microbial communities in Great Salt Lake mats, using both 16S rRNA gene sequencing and metagenomic sequencing, revealed that the dominant organisms are in fact secondary producers, aerobic heterotrophic bacteria that supplement their energy metabolism using light energy via light‐harvesting rhodopsin pigments and other photosynthetic reaction centres (Kanik et al ., 2020).…”

Metagenomic analysis of the soil microbial composition and salt tolerance mechanism in Yuncheng Salt Lake, Shanxi Province

“…Research related to the lake has primarily focused on the human environment, salt tolerant plants, and salt production, yet there are few reports on the microbial diversity and biological mechanisms of salt tolerance in this area ( Huan et al, 2019 ; Ming et al, 2020 ; Gao et al, 2021 ). At the same time, biogeochemical properties affect the composition and distribution of special halophilic and salt-tolerant microbial communities in this area ( Kanik et al, 2020 ). In view of the special nature of the saline environment of Yuncheng Salt Lake, the high-salt soil and the salt lake itself provide excellent opportunities for research on the isolation and screening of salt-tolerant microorganisms and exploring mechanisms of biological salt tolerance.…”