No abstract

Microbial mat communities possess extensive taxonomic and functional diversity, which drive high metabolic rates and rapid cycling of major elements. Modern microbial mats occurring in hypersaline environments are considered as analogs to extinct geobiological formations dating back to ∼ 3.5 Gyr ago. Despite efforts to understand the diversity and metabolic potential of hypersaline microbial mats in Shark Bay, Western Australia, there has yet to be molecular analyses at the transcriptional level in these microbial communities. In this study, we generated metatranscriptomes for the first time from actively growing mats comparing the type of mat, as well as the influence of diel and seasonal cycles. We observed that the overall gene transcription is strongly influenced by microbial community structure and seasonality. The most transcribed genes were associated with tackling the low nutrient conditions by the uptake of fatty acids, phosphorus, iron, and nickel from the environment as well as with protective mechanisms against elevated salinity conditions and to prevent build-up of ammonium produced by nitrate reducing microorganisms. A range of pathways involved in carbon, nitrogen, and sulfur cycles were identified in mat metatranscriptomes, with anoxygenic photosynthesis and chemoautotrophy using the Arnon–Buchanan cycle inferred as major pathways involved in the carbon cycle. Furthermore, enrichment of active anaerobic pathways (e.g., sulfate reduction, methanogenesis, Wood–Ljungdahl) in smooth mats corroborates previous metagenomic studies and further advocates the potential of these communities as modern analogs of ancient microbialites.

Shark Bay, Western Australia, is episodically impacted by tropical cyclones. During 2015, the region was hit by a category 3 cyclone, "severe tropical cyclone Olywn," leading to the formation of a black sludge in an intertidal zone harboring microbial mats and microbialites. Upon returning to the impacted site 12 months later, the black sludge deposit was still recognizable between the microbialite columns and mucilaginous cobbles near the shoreline in the impacted area. Metatranscriptomic and organic geochemical analyses were carried out on the cyclone-derived materials and impacted microbial mat communities to unravel the structure, function, and potential preservation of these deposits following a tropical cyclone. It was found that samples derived from the black sludge contained low relative abundances of cyanobacteria but had higher proportions of heterotrophic and anaerobic microorganisms (e.g., methanogens and sulfate-reducing bacteria). Increased metabolic activity by these microorganisms (e.g., sulfate reduction and organic matter degradation) is thought to drive calcium carbonate precipitation and helps in mat preservation. Comparison of the aliphatic biomarker by gas chromatography-mass spectrometry (GC-MS) analyses showed that C 25 highly branched isoprenoid (HBI) alkenes were significantly higher in the cyclone-derived materials attributed to the relocation of subtidal sediments containing HBI-producing diatom communities by the tropical cyclone. Raney nickel desulfurization of the polar fraction extracted from a mucilaginous cobble revealed sulfur-bound hopanoids and a series of benzohopanes. The presence of these compounds could be indicative of microbial matter that has been influenced by the tropical cyclone which may have caused elevated levels of water column anoxia promoting increased sulfurization of the organic matter to occur.

Storm disturbance and recovery of the peritidal benthic microbial ecosystem occurs as part of the natural climate regime in Shark Bay. However, tropical cyclone and winter storm frequency and intensity are known to be changing due to climate forcing. Presented here is an analysis of the biogeomorphic response of the benthic microbial ecosystem within the intertidal to upper subtidal zone and the beach face coquina deposits of Hamelin Pool, to the passage of Category 3 Severe Tropical Cyclone Olwyn (13 March 2015). Storm effects (initial response to 40 days post‐event) include: erosional sculpting of sediments, mats and structures; deposition and winnowing of sediments; accumulation of mucilaginous products into flocs, slurries and sludges; along with limited development of new coquina deposits in the beach face. Medium (15 months) term observations include: mat recovery and changes with transformation of mucilage deposits into new subtidal gelatinous mats, intertidal transitional mats and low‐elevation microbial structures. Observations suggest that this disturbance had both positive (the floc‐to‐mat biogeomorphic storm response) and negative feedbacks (enhanced bioturbation), which impact the development of stromatolite forming microbial mats and microbialite structures.