Abstract

BackgroundShark Bay, Australia, harbours one of the most extensive and diverse systems of living microbial mats that are proposed to be analogs of some of the earliest ecosystems on Earth. These ecosystems have been shown to possess a substantial abundance of uncultivable microorganisms. These enigmatic microbes, jointly coined as ‘microbial dark matter’ (MDM), are hypothesised to play key roles in modern microbial mats.ResultsWe reconstructed 115 metagenome-assembled genomes (MAGs) affiliated to MDM, spanning 42 phyla. This study reports for the first time novel microorganisms (Zixibacterial order GN15) putatively taking part in dissimilatory sulfate reduction in surface hypersaline settings, as well as novel eukaryote signature proteins in the Asgard archaea. Despite possessing reduced-size genomes, the MDM MAGs are capable of fermenting and degrading organic carbon, suggesting a role in recycling organic carbon. Several forms of RuBisCo were identified, allowing putative CO2 incorporation into nucleotide salvaging pathways, which may act as an alternative carbon and phosphorus source. High capacity of hydrogen production was found among Shark Bay MDM. Putative schizorhodopsins were also identified in Parcubacteria, Asgard archaea, DPANN archaea, and Bathyarchaeota, allowing these members to potentially capture light energy. Diversity-generating retroelements were prominent in DPANN archaea that likely facilitate the adaptation to a dynamic, host-dependent lifestyle.ConclusionsThis is the first study to reconstruct and describe in detail metagenome-assembled genomes (MAGs) affiliated with microbial dark matter in hypersaline microbial mats. Our data suggests that these microbial groups are major players in these systems. In light of our findings, we propose H2, ribose and CO/CO2 as the main energy currencies of the MDM community in these mat systems.Cmbfp_aj5R9yxCxBzxBrnsVideo

Highlights

  • A vast ‘known-unknown’ and even ‘unknown-unknown’, many microorganisms have yet to be unlocked from a majority of Earth’s ecosystems

  • Microbial dark matter metagenome-assembled genomes This study describes for the first time in detail metagenome-assembled genomes (MAGs) associated with microbial dark matter in hypersaline microbial mats

  • One Heimdallarchaeota (Bin_120) and one Lokiarchaeota (Bin_186) MAG had slightly over 10% contamination levels, they are included in this study due to high completeness (> 85%), as well as this being the first Heimdallarchaeota MAG obtained from any microbial mat system

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Summary

Introduction

A vast ‘known-unknown’ and even ‘unknown-unknown’, many microorganisms have yet to be unlocked from a majority of Earth’s ecosystems. Amplicon sequencing revealed that MDM comprises over 15% of the bacterial community and over half of the archaeal population in Shark Bay mats [22, 23] These results have indicated that Shark Bay microbial mats are a huge genetic pool of novel lineages, their functional role(s), including how they adapt to such an extreme environment and their putative interactions with other microorganisms, are still unknown. Shark Bay, Australia, harbours one of the most extensive and diverse systems of living microbial mats that are proposed to be analogs of some of the earliest ecosystems on Earth. These ecosystems have been shown to possess a substantial abundance of uncultivable microorganisms. These enigmatic microbes, jointly coined as ‘microbial dark matter’ (MDM), are hypothesised to play key roles in modern microbial mats

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