Diversity of Bathyarchaeia viruses in metagenomes and virus-encoded CRISPR system components.

Bathyarchaeia represent a class of archaea common and abundant in sedimentary ecosystems. Here we report 56 metagenome-assembled genomes of Bathyarchaeia viruses identified in metagenomes from different environments. Gene sharing network and phylogenomic analyses led to the proposal of four virus families, including viruses of the realms Duplodnaviria and Adnaviria, and archaea-specific spindle-shaped viruses. Genomic analyses uncovered diverse CRISPR elements in these viruses. Viruses of the proposed family "Fuxiviridae" harbor an atypical Type IV-B CRISPR-Cas system and a Cas4 protein that might interfere with host immunity. Viruses of the family "Chiyouviridae" encode a Cas2-like endonuclease and two mini-CRISPR arrays, one with a repeat identical to that in the host CRISPR array, potentially allowing the virus to recruit the host CRISPR adaptation machinery to acquire spacers that could contribute to competition with other mobile genetic elements or to inhibit host defenses. These findings present an outline of the Bathyarchaeia virome and offer a glimpse into their counter-defense mechanisms.

Diversity of Bathyarchaeia viruses in metagenomes and virus-encoded CRISPR system components.

Bathyarchaeia represent a class of archaea common and abundant in sedimentary ecosystems. The virome of Bathyarchaeia so far has not been characterized. Here we report 56 metagenome-assembled genomes of Bathyarchaeia viruses identified in metagenomes from different environments. Gene sharing network and phylogenomic analyses led to the proposal of four virus families, including viruses of the realms Duplodnaviria and Adnaviria, and archaea-specific spindle-shaped viruses. Genomic analyses uncovered diverse CRISPR elements in these viruses. Viruses of the proposed family 'Fuxiviridae' harbor an atypical type IV-B CRISPR-Cas system and a Cas4 protein that might interfere with host immunity. Viruses of the family 'Chiyouviridae' encode a Cas2-like endonuclease and two mini-CRISPR arrays, one with a repeat identical to that in the host CRISPR array, potentially allowing the virus to recruit the host CRISPR adaptation machinery to acquire spacers that could contribute to competition with other mobile genetic elements or to inhibition of host defenses. These findings present an outline of the Bathyarchaeia virome and offer a glimpse into their counter-defense mechanisms.

Genomic and transcriptomic dissection of Theionarchaea in marine ecosystem.

Theionarchaea is a recently described archaeal class within the Euryarchaeota. While it is widely distributed in sediment ecosystems, little is known about its metabolic potential and ecological features. Here, we used metagenomics and metatranscriptomics to characterize 12 theionarchaeal metagenome-assembled genomes, which were further divided into two subgroups, from coastal mangrove sediments of China and seawater columns of the Yap Trench. Genomic analysis revealed that apart from the canonical sulfhydrogenase, Theionarchaea harbor genes encoding heliorhodopsin, group 4 [NiFe]-hydrogenase, and flagellin, in which genes for heliorhodopsin and group 4 [NiFe]-hydrogenase were transcribed in mangrove sediment. Further, the theionarchaeal substrate spectrum may be broader than previously reported as revealed by metagenomics and metatranscriptomics, and the potential carbon substrates include detrital proteins, hemicellulose, ethanol, and CO2. The genes for organic substrate metabolism (mainly detrital protein and amino acid metabolism genes) have relatively higher transcripts in the top sediment layers in mangrove wetlands. In addition, co-occurrence analysis suggested that the degradation of these organic compounds by Theionarchaea might be processed in syntrophy with fermenters (e.g., Chloroflexi) and methanogens. Collectively, these observations expand the current knowledge of the metabolic potential of Theionarchaea, and shed light on the metabolic strategies and roles of these archaea in the marine ecosystems.

Ecological features and global distribution of Asgard archaea.

Asgard is a newly proposed archaeal superphylum, which has been suggested to hold the key to decipher the origin of Eukaryotes. However, their ecology remains largely unknown. Here, we conducted a meta-analysis of publicly available Asgard-associated 16S rRNA gene fragments, and found that just three previously proposed clades (Lokiarchaeota, Thorarchaeota, and Asgard clade 4) are widely distributed, whereas the other seven clades (phylum or class level) are restricted to the sediment biosphere. Asgard archaea, especially Loki- and Thorarchaeota, seem to adapt to marine sediments, and water depth (the depth of the sediment below water surface) and salinity might be crucial factors for the proportion of these microorganisms as revealed by multivariate regression analyses. However, the abundance of Asgard archaea exhibited distinct environmental drivers at the clade-level; for instance, the proportion of Asgard clade 4 was higher in less saline environments (salinity <6.35 psu), while higher for Heimdallarchaeota-AAG and Asgard clade 2 in more saline environment (salinity ≥35 psu). Furthermore, co-occurrence analysis allowed us to find a significant non-random association of different Asgard clades with other groups (e.g., Lokiarchaeota with Deltaproteobacteria and Anaerolineae; Odinarchaeota with Bathyarchaeota), suggesting different interaction potentials among these clades. Overall, these findings reveal Asgard archaea as a ubiquitous group worldwide and provide initial insights into their ecological features on a global scale.

Genomic and transcriptomic insights into methanogenesis potential of novel methanogens from mangrove sediments.

BACKGROUND: Methanogens are crucial to global methane budget and carbon cycling. Methanogens from the phylum Euryarchaeota are currently classified into one class and seven orders, including two novel methanogen taxa, Methanofastidiosa and Methanomassiliicoccales. The relative importance of the novel methanogens to methane production in the natural environment is poorly understood. RESULTS: Here, we used a combined metagenomic and metatranscriptomic approach to investigate the metabolic activity of methanogens in mangrove sediments in Futian Nature Reserve, Shenzhen. We obtained 13 metagenome-assembled genomes (MAGs) representing one class (Methanofastidiosa) and five orders (Methanomassiliicoccales, Methanomicrobiales, Methanobacteriales, Methanocellales, and Methanosarcinales) of methanogens, including the two novel methanogens. Comprehensive annotation indicated the presence of an H2-dependent methylotrophic methanogenesis pathway in Methanofastidiosa and Methanomassiliicoccales. Based on the functional gene analysis, hydrogenotrophic and methylotrophic methanogenesis are the dominant pathways in mangrove sediments. MAG mapping revealed that hydrogenotrophic Methanomicrobiales were the most abundant methanogens and that methylotrophic Methanomassiliicoccales were the most active methanogens in the analyzed sediment profile, suggesting their important roles in methane production. CONCLUSIONS: Partial or near-complete genomes of two novel methanogen taxa, Methanofastidiosa and Methanomassiliicoccales, in natural environments were recovered and analyzed here for the first time. The presented findings highlight the ecological importance of the two novel methanogens and complement knowledge of how methane is produced in mangrove ecosystem. This study implies that two novel methanogens play a vital role in carbon cycle. Video Abstract.

Prokaryotic Diversity in Mangrove Sediments across Southeastern China Fundamentally Differs from That in Other Biomes.

Mangroves, as a blue carbon reservoir, provide an environment for a variety of microorganisms. Mangroves lie in special locations connecting coastal and estuarine areas and experience fluctuating conditions, which are expected to intensify with climate change, creating a need to better understand the relative roles of stochastic and deterministic processes in shaping microbial community assembly. Here, a study of microbial communities inhabiting mangrove sediments across southeastern China, spanning mangroves in six nature reserves, was conducted. We performed high-throughput DNA sequencing of these samples and compared them with data of 1,370 sediment samples collected from the Earth Microbiome Project (EMP) to compare the microbial diversity of mangroves with that of other biomes. Our results showed that prokaryotic alpha diversity in mangroves was significantly higher than that in other biomes and that microbial beta diversity generally clustered according to biome types. The core operational taxonomic units (OTUs) in mangroves were mostly assigned to Gammaproteobacteria, Deltaproteobacteria, Chloroflexi, and Euryarchaeota The majority of beta nearest-taxon index values were higher than 2, indicating that community assembly in mangroves was better explained through a deterministic process than through a stochastic process. Mean annual precipitation (MAP) and total organic carbon (TOC) were main deterministic factors explaining variation in the microbial community. This study fills a gap in addressing the unique microbial diversity of mangrove ecosystems and their microbial community assembly mechanisms.IMPORTANCE Understanding the underlying mechanisms of microbial community assembly patterns is a vital issue in microbial ecology. Mangroves, as an important and special ecosystem, provide a unique environment for examining the relative importance of stochastic and deterministic processes. We made the first global-scale comparison and found that microbial diversity was significantly different in mangrove sediments compared to that of other biomes. Furthermore, our results suggest that a deterministic process is more important in shaping microbial community assembly in mangroves.