Unravelling core microbial metabolisms in the hypersaline microbial mats of Shark Bay using high-throughput metagenomics

Abstract

Modern microbial mats are potential analogues of some of Earth's earliest ecosystems. Excellent examples can be found in Shark Bay, Australia, with mats of various morphologies. To further our understanding of the functional genetic potential of these complex microbial ecosystems, we conducted for the first time shotgun metagenomic analyses. We assembled metagenomic nextgeneration sequencing data to classify the taxonomic and metabolic potential across diverse morphologies of marine mats in Shark Bay. The microbial community across taxonomic classifications using protein-coding and small subunit rRNA genes directly extracted from the metagenomes suggests that three phyla Proteobacteria, Cyanobacteria and Bacteriodetes dominate all marine mats. However, the microbial community structure between Shark Bay and Highbourne Cay (Bahamas) marine systems appears to be distinct from each other. The metabolic potential (based on SEED subsystem classifications) of the Shark Bay and Highbourne Cay microbial communities were also distinct. Shark Bay metagenomes have a metabolic pathway profile consisting of both heterotrophic and photosynthetic pathways, whereas Highbourne Cay appears to be dominated almost exclusively by photosynthetic pathways. Alternative non-rubisco-based carbon metabolism including reductive TCA cycle and 3-hydroxypropionate/4-hydroxybutyrate pathways is highly represented in Shark Bay metagenomes while not represented in Highbourne Cay microbial mats or any other mat forming ecosystems investigated to date. Potentially novel aspects of nitrogen cycling were also observed, as well as putative heavy metal cycling (arsenic, mercury, copper and cadmium). Finally, archaea are highly represented in Shark Bay and may have critical roles in overall ecosystem function in these modern microbial mats.

Coexisting living stromatolites and infaunal metazoans

“…This is argued as a factor which drove the evolution of metazoan mobility, allowing animals to occupy the anoxic, food-rich benthos while moving between and extracting the metabolically beneficial oxygen being formed within the microbialites (Gingras et al 2011). However, this hypothesis is confounded by the anoxic conditions which would develop at night (Des Marais 2003; Mobberley et al 2015) as well as the range of metabolic modes of microbialites, in addition to photoautotrophy (Ruvindy et al 2016). Nonetheless, similar micro-refugia would be present within some modern stromatolites that support metazoans (Table 2), although not strictly assessed in terms of oxygen concentration gradients in the current study, these being accessed through a network of burrows within the matrix (Fig.…”

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

“…However, despite an increasing number of studies indicating archaeal prevalence in some microbial mat systems6132533, the overall role(s) of archaea in microbial mats remains poorly understood. Interestingly, archaea appear to be more abundant in the Shark Bay microbial mats compared to those in open marine ecosystems in the Bahamas13.…”

A year in the life of a thrombolite: comparative metatranscriptomics reveals dynamic metabolic changes over diel and seasonal cycles

“…There are two major categories of microbialites, including stromatolites, with well‐laminated internal structures (Walter, ; Reid et al ., ) and thrombolites, which have irregular clotted fabrics (Aitken, ; Kennard and James, ). Although there has been extensive research on the metabolisms and organisms associated with formation of stromatolites (Visscher et al ., ; Visscher et al ., ; Stolz et al ., ; Burns et al ., ; Papineau et al ., ; Havemann and Foster, ; Allen et al ., ; Baumgartner et al ., ; Foster et al ., ; Foster and Green, ; Goh et al ., ; Berelson et al ., ; Foster and Green, ; Khodadad and Foster, ; Pepe‐Ranney et al ., ; Mata et al ., ; Casaburi et al ., ; Ruvindy et al ., ; Suosaari et al ., ), far fewer studies have examined thrombolite‐forming communities (Desnues et al ., ; Planavsky et al ., ; Myshrall et al ., ; Mobberley et al ., ; Edgcomb et al ., ; Mobberley et al ., ; Gleeson et al ., ; Warden et al ., ; Louyakis et al ., ).…”