Discovery of an Abundance of Biosynthetic Gene Clusters in Shark Bay Microbial Mats

Abstract

Microbial mats are geobiological multilayered ecosystems that have significant evolutionary value in understanding the evolution of early life on Earth. Shark Bay, Australia has some of the best examples of modern microbial mats thriving under harsh conditions of high temperatures, salinity, desiccation, and ultraviolet (UV) radiation. Microorganisms living in extreme ecosystems are thought to potentially encode for secondary metabolites as a survival strategy. Many secondary metabolites are natural products encoded by a grouping of genes known as biosynthetic gene clusters (BGCs). Natural products have diverse chemical structures and functions which provide competitive advantages for microorganisms and can also have biotechnology applications. In the present study, the diversity of BGC were described in detail for the first time from Shark Bay microbial mats. A total of 1477 BGCs were detected in metagenomic data over a 20 mm mat depth horizon, with the surface layer possessing over 200 BGCs and containing the highest relative abundance of BGCs of all mat layers. Terpene and bacteriocin BGCs were highly represented and their natural products are proposed to have important roles in ecosystem function in these mat systems. Interestingly, potentially novel BGCs were detected from Heimdallarchaeota and Lokiarchaeota, two evolutionarily significant archaeal phyla not previously known to possess BGCs. This study provides new insights into how secondary metabolites from BGCs may enable diverse microbial mat communities to adapt to extreme environments.

Conserved bacterial genomes from two geographically isolated peritidal stromatolite formations shed light on potential functional guilds

“…The study of extant stromatolite analogues may help to elucidate the biological mechanisms that led to the formation and evolution of their ancient ancestors. The biogenicity of stromatolites has been studied extensively in the hypersaline and marine formations of Shark Bay, Australia, and Exuma Cay, The Bahamas, respectively (Khodadad and Foster, 2012; Mobberley et al ., 2015; Centeno et al ., 2016; Gleeson et al ., 2016; Ruvindy et al ., 2016; Warden et al ., 2016; White et al ., 2016; Babilonia et al ., 2018; Wong et al ., 2018; Chen et al ., 2020). The presence of Archaea has been noted in several microbial mats and stromatolite systems (Casaburi et al ., 2016; Balci et al ., 2018; Medina‐Chávez et al ., 2019; Chen et al ., 2020), particularly in the stromatolites of Shark Bay, where they are hypothesized to potentially fulfil the role of nitrifiers and hydrogenotrophic methanogens (Wong et al ., 2017).…”

“…The biogenicity of stromatolites has been studied extensively in the hypersaline and marine formations of Shark Bay, Australia, and Exuma Cay, The Bahamas, respectively (Khodadad and Foster, 2012; Mobberley et al ., 2015; Centeno et al ., 2016; Gleeson et al ., 2016; Ruvindy et al ., 2016; Warden et al ., 2016; White et al ., 2016; Babilonia et al ., 2018; Wong et al ., 2018; Chen et al ., 2020). The presence of Archaea has been noted in several microbial mats and stromatolite systems (Casaburi et al ., 2016; Balci et al ., 2018; Medina‐Chávez et al ., 2019; Chen et al ., 2020), particularly in the stromatolites of Shark Bay, where they are hypothesized to potentially fulfil the role of nitrifiers and hydrogenotrophic methanogens (Wong et al ., 2017). Studies of freshwater microbialites in Mexico found that there were significantly more genes associated with phosphate uptake and metabolism than in other communities associated with fresh or marine waters (Breitbart et al ., 2009) and that nitrogen fixation by heterocystous cyanobacteria, sulfur‐reducing bacteria, and purple sulfur bacteria was important to the formation of these particular stromatolites (Falcón et al ., 2007).…”

Metabolic potential of uncultured Antarctic soil bacteria revealed through long-read metagenomic sequencing

“…25% in this survey. Previous short-read metagenomic studies of aquatic and soil environments also reported high numbers of terpene BGCs, with terpenes representing between 15% and 50% of the reported BGCs, respectively [57][58][59] . However, the representativeness of BGC counts obtained through metagenomic studies remains questionable.…”

The ecological roles of microbial lipopeptides: Where are we going?

“…In the ‘microbial mat’ environment microorganisms are exposed to high temperatures, UV radiation and salinity [157] , with a high diversity of NRPS and hybrid NRPS-PKS genes in bacteria of the phyla Planctomycetes, Chloroflexi, Calditrichaeota and for the first time Lokiarchaeota was reported. Lokiarchaeota is an archaeal phyla not previously known to have BGCs, expanding the domain of life to which the future of natural products discovery can take place [158] .…”

“…Microorganisms thrive in a myriad of ‘extreme’ environments, from hot springs and geysers, through to deep sea, hypersaline environments, evaporites, deserts, cold environments (ice, permafrost, and snow) and the Earth’s atmosphere. Given the diversity of genetic machinery recently discovered in microorganisms from Antarctic deserts and microbial matts [140] , [158] , we believe future investigations in a range of ecosystems at the boundaries of life will provide new insights into the ecological roles of LPs [24] . We know that microorganisms exposed to harsh conditions develop biological adaptations, metabolic processes, physiological capabilities and novel strategies to survive, and remain metabolically active in their unique environments [24] .…”