Abstract
Small acidophilic archaea belonging to Micrarchaeota and Parvarchaeota phyla are known to physically interact with some Thermoplasmatales members in nature. However, due to a lack of cultivation and limited genomes on hand, their biodiversity, metabolisms, and physiologies remain largely unresolved. Here, we obtained 39 genomes from acid mine drainage (AMD) and hot spring environments around the world. 16S rRNA gene based analyses revealed that Parvarchaeota were only detected in AMD and hot spring habitats, while Micrarchaeota were also detected in others including soil, peat, hypersaline mat, and freshwater, suggesting a considerable higher diversity and broader than expected habitat distribution for this phylum. Despite their small genomes (0.64–1.08 Mb), these archaea may contribute to carbon and nitrogen cycling by degrading multiple saccharides and proteins, and produce ATP via aerobic respiration and fermentation. Additionally, we identified several syntenic genes with homology to those involved in iron oxidation in six Parvarchaeota genomes, suggesting their potential role in iron cycling. However, both phyla lack biosynthetic pathways for amino acids and nucleotides, suggesting that they likely scavenge these biomolecules from the environment and/or other community members. Moreover, low-oxygen enrichments in laboratory confirmed our speculation that both phyla are microaerobic/anaerobic, based on several specific genes identified in them. Furthermore, phylogenetic analyses provide insights into the close evolutionary history of energy related functionalities between both phyla with Thermoplasmatales. These results expand our understanding of these elusive archaea by revealing their involvement in carbon, nitrogen, and iron cycling, and suggest their potential interactions with Thermoplasmatales on genomic scale.
Highlights
Archaea constitute a considerable portion of microbial diversity, and play significant roles in many biogeochemical cycles on Earth [1]
Two DPANN phyla, Micrarchaeota and Parvarchaeota, referred to as Archaeal Richmond Mine Acidophilic Nanoorganisms (ARMAN), were first reported in acid mine drainage (AMD) biofilms of Iron mountain (Richmond, CA, USA) and are among the smallest microorganisms described to date [8, 9]
ARMAN-specific PCR primers and metagenomics have revealed their occurrence in many other AMD-related environments [14,15,16,17], indicating wide distributions of related microorganisms in nature
Summary
Archaea constitute a considerable portion of microbial diversity, and play significant roles in many biogeochemical cycles on Earth [1]. The recently delineated superphylum DPANN includes several phyla of archaea with small cell and genome sizes and limited metabolic capabilities [3,4,5,6]. 48 DPANN draft genomes are available (Supplementary Table 1; see references therein) and only two symbiotic Nanoarchaeota co-cultures have been obtained [5, 7]. Two DPANN phyla, Micrarchaeota and Parvarchaeota, referred to as Archaeal Richmond Mine Acidophilic Nanoorganisms (ARMAN), were first reported in acid mine drainage (AMD) biofilms of Iron mountain (Richmond, CA, USA) and are among the smallest microorganisms described to date [8, 9]. The AMD biofilms in Iron Mountain have been comprehensively studied for microbial ecology and evolution [10]. ARMAN-specific PCR primers and metagenomics have revealed their occurrence in many other AMD-related environments [14,15,16,17], indicating wide distributions of related microorganisms in nature
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