mSystems最新文献

Giant viruses (GVs) of the phyla Nucleocytoviricota and Mirusviricota are large double-stranded DNA viruses that infect diverse eukaryotic hosts and impact biogeochemical cycles. Their diversity and ecological roles have been well studied in the photic layer of the ocean, but less is known about their activity, population dynamics, and adaptive strategies in the aphotic layers. Here, we conducted eight seasonal time-series samplings of the surface and mesopelagic layers at a coastal site in Muroto, Japan, and integrated 18S metabarcoding, metagenomic, and metatranscriptomic data to investigate mesopelagic GVs and their potential hosts. The analysis identified 48 GV genomes including six that were exclusively detected in the mesopelagic layer. Notably, these mesopelagic-specific GVs showed persistent activity across seasons. To further investigate the distribution and phylogenomic features of GVs at a global scale across broader depths, we compiled 4,473 species-level GV genomes from the OceanDNA MAG project and other resources and analyzed 1,890 marine metagenomes. This revealed 101 deep-sea-specific GVs, distributed across the GV phylogenetic tree, indicating that adaptation to deep-sea environments has occurred in multiple lineages. One clade enriched with deep-sea-specific GVs included a GV genome identified in our Muroto data, which displayed a wide geographic distribution. Seventy-six KEGG orthologs and 74 Pfam domains were specifically enriched in deep-sea-specific GVs, encompassing functions related to the ubiquitin system, energy metabolism, and nitrogen acquisition. These findings support the scenario that distinct GV lineages have adapted to hosts in aphotic marine environments by altering their gene repertoire to thrive in this unique habitat.IMPORTANCEGiant viruses are widespread in the ocean surface and are key in shaping marine ecosystems by infecting phytoplankton and other protists. However, little is known about their activity and adaptive strategies in deep-sea environments. In this study, we performed metagenomic and metatranscriptomic analyses of seawater samples collected from a coastal site in Japan and discovered giant virus genomes showing persistent transcriptional activity across seasons in the mesopelagic water. Using a global marine data set, we further uncovered geographically widespread and vertically extensive groups of deep-sea-specific giant viruses and characterized their distinctive gene repertoire, which likely facilitates adaptation to the limited availability of light and organic compounds in the aphotic zone. These findings expand our understanding of giant virus ecology in the dark ocean.

Global regulators (GRs) are key transcription factors that orchestrate the expression of multiple genes, playing essential roles in stress responses, virulence, secondary metabolism, and antibiotic resistance-traits that make them powerful tools for synthetic biology applications. However, conventional approaches often fail to detect remote homologs and novel GR types, limiting our understanding of their regulatory diversity and evolutionary dynamics across prokaryotes. Here, we present a large-scale, protein language model-driven framework to systematically chart the global regulatory landscape across 14,800 bacterial and archaeal type strain genomes-the most taxonomically diverse prokaryotic data set analyzed to date. Using a deep learning-based GR identification model trained on 74,872 curated GR sequences, we systematically identified over 270,000 GR-like proteins, including 173,256 homologs of 214 experimentally validated GR types, 52 putative GR types, and 76,113 proteins of unknown function. This model demonstrated high sensitivity and generalization capability, enabling the discovery of remote homologs and cryptic regulators beyond the reach of similarity- or domain-based methods. This expanded GR catalog revealed lineage-specific distribution patterns, functionally diverse regulons with both conserved and niche-specific targets, and hierarchical cross-regulatory networks with shared and phylum-enriched hubs. By unveiling the hidden diversity and evolutionary structure of prokaryotic global regulators, this landscape of GRs provides foundational insights into microbial gene regulation and offers a powerful toolkit for the rational design of tunable, modular, and orthogonal genetic circuits in synthetic biology.IMPORTANCEGRs are master transcriptional regulators critical for microbial adaptation, stress tolerance, and metabolic control, and they serve as valuable components for synthetic biology. However, a comprehensive understanding of GR diversity and function across the prokaryotic domain has remained elusive due to the limitations of traditional detection methods. In this study, we developed a deep learning-based identification framework and applied it to 14,800 bacterial and archaeal type strain genomes, resulting in the discovery of over 270,000 GR-like proteins, including dozens of novel types. This work provides a comprehensive landscape of prokaryotic global regulators, revealing lineage-specific distribution patterns, both conserved and specialized regulons, and modular cross-regulatory network architectures. These insights not only deepen our understanding of transcriptional regulation in microbial evolution and ecology but also provide a scalable resource for the rational design of regulatory systems in synthetic biology.

Maladaptive host metabolic responses to infection are emerging as major determinants of infectious disease pathogenesis. However, the factors regulating these metabolic changes within tissues remain poorly understood. In this study, we used toxoplasmosis, as a prototypical example of a disease regulated by strong type I immune responses, to assess the relative roles of current local parasite burden, local tissue inflammation, and the microbiome in shaping local tissue metabolism during acute and chronic infections. Toxoplasmosis is a zoonotic disease caused by the parasite Toxoplasma gondii. This protozoan infects the small intestine and then disseminates broadly in the acute stage of infection, before establishing chronic infection in the skeletal muscle, cardiac muscle, and brain. We compared metabolism in 11 sampling sites in C57BL/6 mice during the acute and chronic stages of T. gondii infection. Strikingly, major spatial mismatches were observed between metabolic perturbation and local parasite burden at the time of sample collection for both disease stages. By contrast, a stronger association with indicators of active type I immune responses was observed, indicating a tighter relationship between metabolic perturbation and local immunity than with local parasite burden. Loss of signaling through the IL1 receptor in IL1R knockout mice was associated with reduced metabolic impact of infection. In addition, we observed significant changes in microbiota composition with infection and candidate microbial origins for multiple metabolites impacted by infection. These findings highlight the metabolic consequences of toxoplasmosis across different organs and potential regulators.IMPORTANCEInflammation is a major driver of tissue perturbation. However, the signals driving these changes on a tissue-intrinsic and molecular level are poorly understood. This study evaluated tissue-specific metabolic perturbations across 11 sampling sites following systemic murine infection with the parasite Toxoplasma gondii. Results revealed relationships between differential metabolite enrichment and variables, including inflammatory signals, pathogen burden, and commensal microbial communities. These data will inform hypotheses about the signals driving specific metabolic adaptation in acute and chronic protozoan infection, with broader implications for infection and inflammation in general.

The DPANN archaea comprise a major microbial lineage that appears to be primarily host dependent. Despite the relative ubiquity of DPANN archaea across the biosphere, our understanding of their ecological role is limited due to the absence of cultivated representatives for most DPANN lineages. The majority of cultivated DPANN species are characterized as mildly parasitic ectosymbionts due to reliance on physical interactions with host cells. However, Candidatus Nanohaloarchaeum antarcticus has been reported to adopt a predatory lifestyle, resulting in the lysis of large numbers of host cells. The factors influencing DPANN-host interactions that drive Ca. Nha. antarcticus to adopt an aggressive lifestyle, although other DPANN appear not to, remain unclear. Here, I present a framework for understanding the ecological pressures specific to the Ca. Nha. antarcticus-Halorubrum lacusprofundi system and why a more aggressive, predatory lifestyle improves population persistence compared with a lifestyle more similar to other DPANN.

The rhizosphere is a critical interface between plant roots and soil, harboring diverse microbial communities that are essential to plant and ecosystem health. Although these communities exhibit stark temporal dynamics, their dormancy/activity transitions remain poorly understood. Such transitions may enable microbes to rapidly adjust functional contributions faster than community turnover alone would allow. Here, we used RNA metabarcoding to characterize the active fraction of microbial communities on the roots of quaking aspen (Populus tremuloides) in a time-series study across a natural environmental gradient. We explore cryptic temporal microbial community dynamics of rhizosphere communities at the ecosystem scale. The active rhizosphere bacterial and fungal communities were more temporally dynamic than total communities, while total communities exhibited a stronger response to site-specific conditions. Notably, some core microbiome members were often inactive, yielding a smaller "active core" subset. The fungal endophyte Hyaloscypha finlandica was the only microbe that was both present and active in all plots across all timepoints. Soil temperature strongly influenced both total and active community composition, with the fungal class Eurotiomycetes showing a temperature-dependent seasonal decline in abundance. Together, these results reveal that modulation of microbial activity levels is a key mechanism by which the plant root holobiont responds to environmental variation, and that even dominant symbionts may frequently persist in dormancy within the rhizosphere.

Importance: Members of the rhizosphere exhibit dynamic patterns of activity and dormancy. This study stresses the need to focus on active microbial communities to detect temporal changes in plant microbiomes. Additionally, the metabolic activity of microbes should be considered a key determinant of core microbiome membership. Parallel patterns in active community dynamics between fungal and bacterial communities provide a potentially generalizable rule of microbial community temporal dynamics in plant rhizospheres.

Microbiome research focusing on late and moderate preterm infants (LMPT; 32 to 36 weeks gestation) is limited, despite rising LMPT births, large healthcare burdens, and increased risks of multiple morbidities, potentially microbially related. In this longitudinal cohort study, 16S rRNA gene sequencing was used to analyze 371 stool and 402 saliva samples from 160 LMPT infants, collected at five time points between birth and 12 months corrected age (CA), to describe spatial and temporal variability in gut and oral microbiomes. Paired stool and saliva samples (n = 337) were analyzed for potential microbial relationships. Early LMPT samples (up to 60 days of life; DOL) were also compared with data from seven extremely preterm infants (EP; <28 weeks gestation; stool n = 14, saliva n = 14). LMPT stool and saliva were composed of distinct microbial communities at each time point, and both sample types showed increasing alpha diversity over time. Stool was initially dominated by Escherichia/Shigella, Klebsiella, and Streptococcus, with Bifidobacterium becoming dominant from term equivalent age (TEA). Contrarily, saliva was dominated by Streptococcus throughout the first year, with early contributions from Staphylococcus and later Veillonella. LMPT infants had higher stool and lower saliva diversity compared with EP infants. Both sample types from EP infants were taxonomically distinct from LMPTs, with Escherichia/Shigella dominating both EP sample types throughout the first 60 DOL. The results highlight the unique trajectories of LMPT microbiomes and emphasize the role of gestational maturity in shaping microbial communities.IMPORTANCEThe oral and gut microbiome develops from birth and plays important roles in health. This has been well studied in extremely preterm infants (EP; born <32 weeks gestation) and term infants (born >38 weeks gestation), but there is a paucity of research describing oral and gut microbiome development in late and moderate preterm infants (LMPT; 32 to 36 weeks gestation). Our study analyzed microbiome development in 160 LMPT infants from birth to 12 months corrected age. The results showed distinct microbial communities in stool and saliva, with increasing alpha diversity and niche specification over time. LMPT infants' gut microbiome became dominated by Bifidobacterium by month 3, while the oral community was consistently dominated by Streptococcus. These results highlight that LMPT infants have gut and oral microbiome development that is more like term infants than EP infants, which has important implications for the care of LMPT infants.

Microbial biomineralization is a fundamental driver of global biogeochemical cycles, yet the ability of prokaryotes to form intracellular carbonates remains rarely documented. Here, we report three ecotypes of magnetotactic bacteria (MTB) affiliated with the Pseudomonadota and the deep-branching Nitrospirota phyla that concurrently synthesize magnetite magnetosomes and intracellular calcium carbonate inclusions enriched in Ba, Mg, and Ni. These carbonate granules are typically spherical and contrast with the highly ordered morphology of magnetite crystals. Comparative genomic analyses reveal that these MTB encode multiple metal-permease systems (e.g., GDT1, CorA, ZnuA2), which suggests both a capacity for selective uptake of divalent cations from their environment and a process likely linked to intracellular carbonate precipitation. By uncovering new examples of bacterial intracellular calcification, our findings expand the known diversity and genetic basis of prokaryotic biomineralization. Moreover, they highlight a potential role of MTB in mediating heavy-metal cycling and provide a refined framework for understanding microbially driven carbonate formation.

Importance: Intracellular biomineralization is a hallmark of animals and algae, yet among prokaryotes, it has traditionally been associated with a limited range of lineages and minerals. This study reveals that magnetotactic bacteria (MTB) from both the Pseudomonadota and the deep-branching Nitrospirota phyla are capable of intracellularly forming carbonate granules enriched in diverse divalent cations, including environmentally scarce trace metals Ba²⁺ and Ni²⁺, and biologically essential Mg²⁺. These findings significantly expand the known taxonomic and functional diversity of prokaryotic intracellular calcifiers. By integrating electron microscopy, metagenomics, and structural protein modeling, we propose a potential metal-selective transport system that facilitates trace element accumulation and carbonate precipitation. This work establishes a previously underappreciated role for MTB in trace metal biogeochemical cycling (i.e., Ba²⁺ and Ni²⁺) and suggests that intracellular calcification may be a more widespread bacterial trait than previously assumed.