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Although ammonia-oxidizing archaea (AOA) are globally distributed in nature, growth in biofilms has been relatively little explored. Here, we investigated six representatives of three different terrestrial and marine clades of AOA in a longitudinal and quantitative study for their ability to form biofilm, and studied gene expression patterns of three representatives. Although all strains grew on a solid surface, soil strains of the genera Nitrosocosmicus and Nitrososphaera exhibited the highest capacity for biofilm formation. Based on microscopic and gene expression data, two different colonization strategies could be distinguished. S-layer containing AOA (from both soil and marine habitats) initialized attachment as single cells, subsequently forming denser layers, whereas the S-layer free species of the Nitrosocosmicus clade attached as suspended aggregates to the surface and henceforth showed fastest establishment of biofilm. Transcription profiles were significantly different between planktonic and biofilm growth in all strains, and revealed individual transcriptomic responses, albeit fulfilling shared functions. In particular, the strong expression of different types of multicopper oxidases was observed in all strains suggesting modifications of their cell coats. S-layer carrying AOA each additionally expressed a set of adhesion proteins supporting attachment. Detoxification of nitrous compounds, copper acquisition as well as the expression of transcription factor B were also shared responses among biofilm producing strains. However, the majority of differentially expressed protein families was distinct among the three strains, illustrating that individual solutions have evolved for the shared growth mode of biofilm formation in AOA, probably driven by the different ecological niches.

The CPR and DPANN superphyla are globally distributed in anoxic habitats including extreme environments. However, the biogeography and potential ecological functions of their viruses remain unexplored. Here, we recover diverse CPR/DPANN metagenomic viral genomes from 90 acid mine drainage (AMD) sediments sampled across southeast China. Our data reveal deterministic processes as the primary driver of virome assembly shaping the distinct distribution patterns of CPR and DPANN viruses. While lifestyle prediction shows higher lytic virus diversity associated with DPANN, both CPR/DPANN viruses likely use the Piggyback-the-winner (PtW) strategy to co-exist with hosts in AMD sediments, with CPR viromes exhibiting increased lysis in low host-density regimes under intensive acidity/salinity conditions. A subsequent metatranscriptomic analysis uncovers diverse functional genes encoded by CPR and DPANN viruses actively expressed in situ, potentially supplementing host metabolisms yet diverging in replication, transcription, and translation-related functions. Furthermore, partial correlation network analysis suggests that putative symbiotic hosts of the CPR/DPANN may confer protection against viral infection through enhanced antiviral defense. Our results highlight the complex interplays between viruses, DPANN and CPR organisms, and their symbiotic hosts. The ecological role of viruses for CPR bacteria and DPANN archaea remains understudied. Here, the authors apply metagenomic approaches to study the biogeographic distribution of CPR and DPANN viruses in acid mine drainage sediments and elucidate their complex interplays.

Chen, L.-X., Méndez-García, C., Dombrowski, N., Servín-Garcidueñas, L.E., Eloe-Fadrosh, E.A., Fang, B.-Z., Luo, Z.-H., Tan, S., Zhi, X.-Y., Hua, Z.-S., Martinez-Romero, E., Woyke, T., Huang, L.-N., Sánchez, J., Peláez, A.I., Ferrer, M., Baker, B.J., Shu, W.-S.

Candidate phyla radiation (CPR) bacteria and DPANN archaea constitute a significant fraction of Earth’s prokaryotic diversity. Despite their ubiquity and abundance, especially in anoxic habitats, we know little about the community patterns and ecological drivers of these ultra-small, putatively episymbiotic microorganisms across geographic ranges. This study is facilitated by a large collection of CPR and DPANN metagenome-assembled genomes recovered from the metagenomes of 90 sediments sampled from geochemically diverse acid mine drainage (AMD) environments across southeast China. Our comprehensive analyses have allowed first insights into the biogeographic patterns and functional differentiation of these major enigmatic prokaryotic groups in the AMD model system.

Ammonia-oxidizing Nitrososphaeria are among the most abundant archaea on Earth and have profound impacts on the biogeochemical cycles of carbon and nitrogen. In contrast to these well-studied ammonia-oxidizing archaea (AOA), deep-branching non-AOA within this class remain poorly characterized because of a low number of genome representatives. Here, we reconstructed 128 Nitrososphaeria metagenome-assembled genomes from acid mine drainage and hot spring sediment metagenomes. Comparative genomics revealed that extant non-AOA are functionally diverse, with capacity for carbon fixation, carbon monoxide oxidation, methanogenesis, and respiratory pathways including oxygen, nitrate, sulfur, or sulfate, as potential terminal electron acceptors. Despite their diverse anaerobic pathways, evolutionary history inference suggested that the common ancestor of Nitrososphaeria was likely an aerobic thermophile. We further surmise that the functional differentiation of Nitrososphaeria was primarily shaped by oxygen, pH, and temperature, with the acquisition of pathways for carbon, nitrogen, and sulfur metabolism. Our study provides a more holistic and less biased understanding of the diversity, ecology, and deep evolution of the globally abundant Nitrososphaeria.

Candidatus Acidulodesulfobacterales, a formerly proposed bacterial order within the Deltaproteobacteria lineage, represents an ecologically significant group in sulfur-rich environments. Their diversity and functional potential in artificial acid mine drainage (AMD) ecosystems have been well studied; however, their distribution and ecological role in marine hydrothermal sulfides remain poorly understood. Here we integrated publicly available metagenome-assembled genomes (MAGs) with a newly reconstructed MAG from hydrothermal sulfides to perform comprehensive phylogenetic, metabolic, and host-virus interaction analyses. Phylogenomic and 16S rRNA gene analyses indicated that this lineage represents a distinct phylum-level clade, leading us to propose the designation Ca . Acidulodesulfobacteriota. Metabolic reconstructions indicated a versatile lifestyle, encompassing pathways for carbon fixation, nitrogen fixation, sulfur metabolism, iron oxidation, and hydrogen oxidation. Notably, the concatenated DsrAB protein phylogeny and the mixed enzyme types involved in Dsr-dependent dissimilatory sulfur metabolism suggest that Ca . Acidulodesulfobacteriota may represent a transitional lineage in the evolutionary shift from reductive to oxidative Dsr metabolism. Viral auxiliary metabolic genes (AMGs) associated with this phylum were predicted to modulate host metabolic pathways, including folate biosynthesis and sulfur metabolism, highlighting intricate host-virus interactions. These findings advance our understanding of the evolution, metabolic potential, and ecological roles of Ca . Acidulodesulfobacteriota in biogeochemical cycling.

Wild animals may encounter multiple challenges especially food shortage and altered diet composition in their suboptimal ranges. Yet, how the gut microbiome responds to dietary changes remains poorly understood. Prior studies on wild animal microbiomes have typically leaned upon relatively coarse dietary records and individually unresolved fecal samples. Here, we conducted a longitudinal study integrating 514 time-series individually recognized fecal samples with parallel fine-grained dietary data from two Skywalker hoolock gibbon (Hoolock tianxing) groups populating high-altitude mountainous forests in western Yunnan Province, China. 16S rRNA gene amplicon sequencing showed a remarkable seasonal fluctuation in the gibbons’ gut microbial community structure both across individuals and between the social groups, especially driven by the relative abundances of Lanchnospiraceae and Oscillospiraceae associated with fluctuating consumption of leaf. Metagenomic functional profiling revealed that diverse metabolisms associated with cellulose degradation and short-chain fatty acids (SCFAs) production were enriched in the high-leaf periods possibly to compensate for energy intake. Genome-resolved metagenomics further enabled the resolving metabolic capacities associated with carbohydrate breakdown among community members which exhibited a high degree of functional redundancy. Our results highlight a taxonomically and functionally sensitive gut microbiome actively responding to the seasonally shifting diet, facilitating the survival and reproduction of the endangered gibbon species in their suboptimal habitats.

Background Candidatus Nanohaloarchaeota, an archaeal phylum within the DPANN superphylum, is characterized by limited metabolic capabilities and limited phylogenetic diversity and until recently has been considered to exclusively inhabit hypersaline environments due to an obligate association with Halobacteria . Aside from hypersaline environments, Ca. Nanohaloarchaeota can also have been discovered from deep-subsurface marine sediments. Results Three metagenome-assembled genomes (MAGs) representing a new order within the Ca. Nanohaloarchaeota were reconstructed from a stratified salt crust and proposed to represent a novel order, Nucleotidisoterales . Genomic features reveal them to be anaerobes capable of catabolizing nucleotides by coupling nucleotide salvage pathways with lower glycolysis to yield free energy. Comparative genomics demonstrated that these and other Ca. Nanohaloarchaeota inhabiting saline habitats use a “salt-in” strategy to maintain osmotic pressure based on the high proportion of acidic amino acids. In contrast, previously described Ca. Nanohaloarchaeota MAGs from geothermal environments were enriched with basic amino acids to counter heat stress. Evolutionary history reconstruction revealed that functional differentiation of energy conservation strategies drove diversification within Ca. Nanohaloarchaeota, further leading to shifts in the catabolic strategy from nucleotide degradation within deeper lineages to polysaccharide degradation within shallow lineages. Conclusions This study provides deeper insight into the ecological functions and evolution of the expanded phylum Ca. Nanohaloarchaeota and further advances our understanding on the functional and genetic associations between potential symbionts and hosts. 6R3_PbsEzFSPy16NiyaaD4 Video Abstract

Little is known about the regulation of carbon metabolism within ammonia-oxidizing archaea (AOA), a widespread clade that plays a critical role in the global nitrogen cycle while also fixing inorganic carbon. To address this missing knowledge, the soil AOA Nitrososphaera viennensis was subjected to various levels of inorganic carbon and analyzed via a systems biology approach to better understand how its core metabolism is regulated. The results demonstrate a strong dependence on the carbon fixation cycle and highlight key connection points between the core metabolic pathways. The analysis additionally revealed tight control on translational processes and elucidated unique cellular responses when the organism was exposed to either exogenous catalase or pyruvate to relieve oxidative stress from reactive oxygen species. The presented data highlight metabolic responses of N. viennensis and provide a better understanding of how the organism, and likely other AOA, respond to various environmental conditions.

Mining is among the human activities with widest environmental impacts, and mining-impacted environments are characterized by high levels of metals that can co-select for antibiotic resistance genes (ARGs) in microorganisms. However, ARGs in mining-impacted environments are still poorly understood. Here, we conducted a comprehensive study of ARGs in such environments worldwide, taking advantage of 272 metagenomes generated from a global-scale data collection and two national sampling efforts in China. The average total abundance of the ARGs in globally distributed studied mine sites was 1572 times per gigabase, being rivaling that of urban sewage but much higher than that of freshwater sediments. Multidrug resistance genes accounted for 40% of the total ARG abundance, tended to co-occur with multimetal resistance genes, and were highly mobile (e.g. on average 16% occurring on plasmids). Among the 1848 high-quality metagenome-assembled genomes (MAGs), 85% carried at least one multidrug resistance gene plus one multimetal resistance gene. These high-quality ARG-carrying MAGs considerably expanded the phylogenetic diversity of ARG hosts, providing the first representatives of ARG-carrying MAGs for the Archaea domain and three bacterial phyla. Moreover, 54 high-quality ARG-carrying MAGs were identified as potential pathogens. Our findings suggest that mining-impacted environments worldwide are underexplored hotspots of multidrug resistance genes.