Abstract

Stromatolites are organosedimentary build-ups that have formed as a result of the sediment trapping, binding and precipitating activities of microbes. Today, extant systems provide an ideal platform for understanding the structure, composition, and interactions between stromatolite-forming microbial communities and their respective environments. In this study, we compared the metagenomes of three prevalent stromatolite-forming microbial mat types in the Spaven Province of Hamelin Pool, Shark Bay located in Western Australia. These stromatolite-forming mat types included an intertidal pustular mat as well as a smooth and colloform mat types located in the subtidal zone. Additionally, the metagenomes of an adjacent, non-lithifying mat located in the upper intertidal zone were also sequenced for comparative purposes. Taxonomic and functional gene analyses revealed distinctive differences between the lithifying and non-lithifying mat types, which strongly correlated with water depth. Three distinct populations emerged including the upper intertidal non-lithifying mats, the intertidal pustular mats associated with unlaminated carbonate build-ups, and the subtidal colloform and smooth mat types associated with laminated structures. Functional analysis of metagenomes revealed that amongst stromatolite-forming mats there was an enrichment of photosynthesis pathways in the pustular stromatolite-forming mats. In the colloform and smooth stromatolite-forming mats, however, there was an increase in the abundance of genes associated with those heterotrophic metabolisms typically associated with carbonate mineralization, such as sulfate reduction. The comparative metagenomic analyses suggest that stromatolites of Hamelin Pool may form by two distinctive processes that are highly dependent on water depth. These results provide key insight into the potential adaptive strategies and synergistic interactions between microbes and their environments that may lead to stromatolite formation and accretion.

Highlights

  • Stromatolites are one of the most prevalent and recognizable components of the fossil record, dating back more than 3.7 Ga years (Grotzinger and Knoll, 1999; Nutman et al, 2016)

  • Hamelin Pool represents the largest known marine habitat for actively accreting stromatolites; little is known about the molecular pathways underlying the different stromatolite-forming mat types in this ecosystem

  • The results of this study provide evidence that: (1) the stromatolite-forming mats types have distinct taxonomic and functional gene profiles compared to non-lithifying mats; (2) colloform and smooth stromatoliteforming mats exhibit distinctive surface morphologies, yet show few taxonomic and functional gene differences; and (3) intertidal pustular stromatolite-forming mats are enriched in photosynthetic genes compared to the colloform and smooth stromatolite-forming mats, suggesting two distinctive metabolic processes driving stromatolite formation within Hamelin Pool

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Summary

Introduction

Stromatolites are one of the most prevalent and recognizable components of the fossil record, dating back more than 3.7 Ga years (Grotzinger and Knoll, 1999; Nutman et al, 2016) These lithified, organosedimentary structures are a type of microbialite, formed by the sediment trapping, binding and/or carbonate precipitating activities of microorganisms in response to their local environment (Awramik et al, 1976; Burne and Moore, 1987). Stromatolites are distinguished from other microbialites by the presence of laminated microstructures, which are formed through iterative successions of sedimentation, microbial mat growth, and lithification (Reid et al, 2000; Dupraz and Visscher, 2005; Pace et al, 2018) These long-lived microbialite ecosystems have had a profound impact on the habitability of the planet, as they are attributed to changing the global redox conditions via oxygenic photosynthesis (Des Marais, 1991; Lyons et al, 2014). Modern microbialite ecosystems are widespread and are found in a diverse range of environments including, but not limited to, lacustrine ecosystems (e.g., Cuatro Ciénegas, Mexico; Lake Alchichica, Mexico; Pavilion and Kelly Lake, British Columbia) (Osborne et al, 1982; Ferris et al, 1997; Laval et al, 2000; Souza et al, 2006; Couradeau et al, 2011; Theisen et al, 2015; Chagas et al, 2016; White et al, 2016), freshwater systems (e.g., Deer Cave and Giblin River; Lundberg and McFarlane, 2011; Proemse et al, 2017); geothermal springs (e.g., Yellowstone National Park, WY, United States) (Inskeep et al, 2004; PepeRanney et al, 2012), open marine environments (e.g., Exuma Sound, The Bahamas) (Dravis, 1983; Dill et al, 1986; Reid et al, 2000; Khodadad and Foster, 2012), and hypersaline waters (e.g., Kiritimati Atoll, Great Salt Lake) (Burns et al, 2004; Schneider et al, 2013; Ruvindy et al, 2016; Suosaari et al, 2016a; Lindsay et al, 2017)

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