Dynamics of archaea at fine spatial scales in Shark Bay mat microbiomes

Abstract

The role of archaea in microbial mats is poorly understood. Delineating the spatial distribution of archaea with mat depth will enable resolution of putative niches in these systems. In the present study, high throughput amplicon sequencing was undertaken in conjunction with analysis of key biogeochemical properties of two mats (smooth and pustular) from Shark Bay, Australia. One-way analysis of similarity tests indicated the archaeal community structures of smooth and pustular mats were significantly different (global R = 1, p = 0.1%). Smooth mats possessed higher archaeal diversity, dominated by Parvarchaeota. The methanogenic community in smooth mats was dominated by hydrogenotrophic Methanomicrobiales, as well as methylotrophic Methanosarcinales, Methanococcales, Methanobacteriales and Methanomassiliicoccaceae. Pustular mats were enriched with Halobacteria and Parvarchaeota. Key metabolisms (bacterial and archaeal) were measured, and the rates of oxygen production/consumption and sulfate reduction were up to four times higher in smooth than in pustular mats. Methane production peaked in the oxic layers and was up to seven-fold higher in smooth than pustular mats. The finding of an abundance of anaerobic methanogens enriched at the surface where oxygen levels were highest, coupled with peak methane production in the oxic zone, suggests putative surface anoxic niches in these microbial mats.

Disentangling the drivers of functional complexity at the metagenomic level in Shark Bay microbial mat microbiomes

“…Furthermore, Shark Bay microbial mats are subject to hypersalinity of more than 60 PSU [3,5], desiccation stress, and high UV radiation [18,19]. Daily tidal cycles also cause fluctuations in salinity and temperature at a local scale in the mat microenvironment [20,21], adding another dimension to the extreme conditions present. The Shark Bay microbial mat systems are thus considered as an ecological model for understanding stress response and resilience in microbial ecosystems, as well as a window to the past.…”

“…Early work in Shark Bay has focused primarily on understanding microbial diversity using targeted culturing and cloning/sequencing of 16S rDNA PCR products [2,4]. These studies proposed the Shark Bay systems were dominated by Proteobacteria, Bacteroidetes, Cyanobacteria, and Haloarchaea [2,4], and, more recently, deep iTag amplicon sequencing has revealed another dominant clade -Chloroflexi-as well as novel members, including OP8, GN04, and Parvarchaeota [3,21,22]. These latter studies were coupled with microelectrode measurements in Shark Bay and indicated a steep biogeochemical gradient with vertical depth in the microbial mats (O 2 , H 2 S, CH 4 ) [3,21,23].…”

“…These studies proposed the Shark Bay systems were dominated by Proteobacteria, Bacteroidetes, Cyanobacteria, and Haloarchaea [2,4], and, more recently, deep iTag amplicon sequencing has revealed another dominant clade -Chloroflexi-as well as novel members, including OP8, GN04, and Parvarchaeota [3,21,22]. These latter studies were coupled with microelectrode measurements in Shark Bay and indicated a steep biogeochemical gradient with vertical depth in the microbial mats (O 2 , H 2 S, CH 4 ) [3,21,23]. It has been proposed that microbial interactions and biochemical cycling occur at a fine, millimeter scale [6], and steep nutrient gradients support niche differentiation, allowing different microorganisms to interact with each other and the environment in their specialized niche [24,25].…”

Microbial diversity and biomarker analysis of modern freshwater microbialites from Laguna Bacalar, Mexico

“…Modern microbialites have been extensively studied using lipid biomarker analysis, gene sequencing, isotopic analysis, growth experiments, and microelectrode measurements from a wide range of sites, including Shark Bay in Western Australia (Allen, Neilan, Burns, Jahnke, & Summons, 2010;Goh et al, 2009;Grice et al, 2014;Ruvindy, White, Neilan, & Burns, 2015;Wong, Smith, Visscher, & Burns, 2015;Wong et al, 2017), the Bahamas (Andres & Pamela Reid, 2006;Baumgartner et al, 2006;Dupraz, Fowler, Tobias, & Visscher, 2013;Mobberley et al, 2015;Paerl, Steppe, & Reid, 2001;Reid et al, 2000;Visscher et al, 1998), Yellowstone National Park USA (Jahnke et al, 2004;Osburn, Sessions, Pepe-Ranney, & Spear, 2011;Pepe-Ranney et al, 2012), Pavilion Lake in British Columbia Canada (Brady, Laval, Lim, & Slater, 2014;Russell et al, 2014;White et al, 2016), the Antarctic McMurdo Ice Shelf (Jungblut, Allen, Burns, & Neilan, 2009), and Alchichica, Mexico (Breitbart et al, 2009;Couradeau et al, 2011). The study of modern microbialites enhances our understanding of ancient analogs by connecting explicit biosignatures such as DNA and RNA sequences and aqueous geochemistry to those that are preserved over geologic time such as carbonate morphology and lipid biomarkers.…”

Bioinformatic, phylogenetic and chemical analysis of the UV‐absorbing compounds scytonemin and mycosporine‐like amino acids from the microbial mat communities of Shark Bay, Australia

“…Despite their strikingly different morphologies, these mats share many bacterial, archaeal and eukaryotic phyla (Allen et al, 2009). Recent community sequencing analyses have characterized in particular the bacterial and archaeal functional diversity of Hamelin Pool microbial mats (Wong et al, 2015;Wong et al, 2017;Wong et al, 2018), with a range of different phototrophs present. The smooth mats feature a smooth, light brown surface while pustular mats are characterized by a dark pigmented and pustular surface layer.…”