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ABSTRACT Creating and maintaining an appropriate chemical environment is essential for biomineralization, the process by which organisms precipitate minerals to form their shells or skeletons, yet the mechanisms involved in maintaining calcifying fluid chemistry are not fully defined. In particular, the role of microorganisms in facilitating or hindering animal biomineralization is poorly understood. Here, we investigated the taxonomic diversity and functional potential of microbial communities inhabiting oyster calcifying fluid. We used shotgun metagenomics to survey calcifying fluid microbial communities from three different oyster harvesting sites. There was a striking consistency in taxonomic composition across the three collection sites. We also observed archaea and viruses that had not been previously identified in oyster calcifying fluid. Furthermore, we identified microbial energy-conserving metabolisms that could influence the host’s calcification, including genes involved in sulfate reduction and denitrification that are thought to play pivotal roles in inorganic carbon chemistry and calcification in microbial biofilms. These findings provide new insights into the taxonomy and functional capacity of oyster calcifying fluid microbiomes, highlighting their potential contributions to shell biomineralization, and contribute to a deeper understanding of the interplay between microbial ecology and biogeochemistry that could potentially bolster oyster calcification. IMPORTANCEPrevious research has underscored the influence of microbial metabolisms in carbonate deposition throughout the geological record. Despite the ecological importance of microbes to animals and inorganic carbon transformations, there have been limited studies characterizing the potential role of microbiomes in calcification by animals such as bivalves. Here, we use metagenomics to investigate the taxonomic diversity and functional potential of microbial communities in calcifying fluids from oysters collected at three different locations. We show a diverse microbial community that includes bacteria, archaea, and viruses, and we discuss their functional potential to influence calcifying fluid chemistry via reactions like sulfate reduction and denitrification. We also report the presence of carbonic anhydrase and urease, both of which are critical in microbial biofilm calcification. Our findings have broader implications in understanding what regulates calcifying fluid chemistry and consequentially the resilience of calcifying organisms to 21st century acidifying oceans. 

<bold>Abstract</bold> Deciphering the relationship between a gene and its genomic context is fundamental to understanding and engineering biological systems. Machine learning has shown promise in learning latent relationships underlying the sequence-structure-function paradigm from massive protein sequence datasets. However, to date, limited attempts have been made in extending this continuum to include higher order genomic context information. Evolutionary processes dictate the specificity of genomic contexts in which a gene is found across phylogenetic distances, and these emergent genomic patterns can be leveraged to uncover functional relationships between gene products. Here, we train a genomic language model (gLM) on millions of metagenomic scaffolds to learn the latent functional and regulatory relationships between genes. gLM learns contextualized protein embeddings that capture the genomic context as well as the protein sequence itself, and encode biologically meaningful and functionally relevant information (e.g. enzymatic function, taxonomy). Our analysis of the attention patterns demonstrates that gLM is learning co-regulated functional modules (i.e. operons). Our findings illustrate that gLM’s unsupervised deep learning of the metagenomic corpus is an effective and promising approach to encode functional semantics and regulatory syntax of genes in their genomic contexts and uncover complex relationships between genes in a genomic region. 

We assessed the relationship between rates of biological energy utilization and the biomass sustained by that energy utilization, at both the organism and biosphere level. We compiled a dataset comprising >10,000 basal, field, and maximum metabolic rate measurements made on >2,900 individual species, and, in parallel, we quantified rates of energy utilization, on a biomass-normalized basis, by the global biosphere and by its major marine and terrestrial components. The organism-level data, which are dominated by animal species, have a geometric mean among basal metabolic rates of 0.012 W (g C)⁻¹and an overall range of more than six orders of magnitude. The biosphere as a whole uses energy at an average rate of 0.005 W (g C)⁻¹but exhibits a five order of magnitude range among its components, from 0.00002 W (g C)⁻¹for global marine subsurface sediments to 2.3 W (g C)⁻¹for global marine primary producers. While the average is set primarily by plants and microorganisms, and by the impact of humanity upon those populations, the extremes reflect systems populated almost exclusively by microbes. Mass-normalized energy utilization rates correlate strongly with rates of biomass carbon turnover. Based on our estimates of energy utilization rates in the biosphere, this correlation predicts global mean biomass carbon turnover rates of ~2.3 y⁻¹for terrestrial soil biota, ~8.5 y⁻¹for marine water column biota, and ~1.0 y⁻¹and ~0.01 y⁻¹for marine sediment biota in the 0 to 0.1 m and >0.1 m depth intervals, respectively. 

Abstract Many microbes in nature reside in dense, metabolically interdependent communities. We investigated the nature and extent of microbe-virus interactions in relation to microbial density and syntrophy by examining microbe-virus interactions in a biomass dense, deep-sea hydrothermal mat. Using metagenomic sequencing, we find numerous instances where phylogenetically distant (up to domain level) microbes encode CRISPR-based immunity against the same viruses in the mat. Evidence of viral interactions with hosts cross-cutting microbial domains is particularly striking between known syntrophic partners, for example those engaged in anaerobic methanotrophy. These patterns are corroborated by proximity-ligation-based (Hi-C) inference. Surveys of public datasets reveal additional viruses interacting with hosts across domains in diverse ecosystems known to harbour syntrophic biofilms. We propose that the entry of viral particles and/or DNA to non-primary host cells may be a common phenomenon in densely populated ecosystems, with eco-evolutionary implications for syntrophic microbes and CRISPR-mediated inter-population augmentation of resilience against viruses. 

ABSTRACT Some marine microbes are seemingly “ubiquitous,” thriving across a wide range of environmental conditions. While the increased depth in metagenomic sequencing has led to a growing body of research on within-population heterogeneity in environmental microbial populations, there have been fewer systematic comparisons and characterizations of population-level genetic diversity over broader expanses of time and space. Here, we investigated the factors that govern the diversification of ubiquitous microbial taxa found within and between ocean basins. Specifically, we use mapped metagenomic paired reads to examine the genetic diversity of ammonia-oxidizing archaeal (“ Candidatus Nitrosopelagicus brevis”) populations in the Pacific (Hawaii Ocean Time-series [HOT]) and Atlantic (Bermuda Atlantic Time Series [BATS]) Oceans sampled over 2 years. We observed higher nucleotide diversity in “ Ca. N. brevis” at HOT, driven by a higher rate of homologous recombination. In contrast, “ Ca. N. brevis” at BATS featured a more open pangenome with a larger set of genes that were specific to BATS, suggesting a history of dynamic gene gain and loss events. Furthermore, we identified highly differentiated genes that were regulatory in function, some of which exhibited evidence of recent selective sweeps. These findings indicate that different modes of genetic diversification likely incur specific adaptive advantages depending on the selective pressures that they are under. Within-population diversity generated by the environment-specific strategies of genetic diversification is likely key to the ecological success of “ Ca. N. brevis.” IMPORTANCE Ammonia-oxidizing archaea (AOA) are one of the most abundant chemolithoautotrophic microbes in the marine water column and are major contributors to global carbon and nitrogen cycling. Despite their ecological importance and geographical pervasiveness, there have been limited systematic comparisons and characterizations of their population-level genetic diversity over time and space. Here, we use metagenomic time series from two ocean observatories to address the fundamental questions of how abiotic and biotic factors shape the population-level genetic diversity and how natural microbial populations adapt across diverse habitats. We show that the marine AOA “ Candidatus Nitrosopelagicus brevis” in different ocean basins exhibits distinct modes of genetic diversification in response to their selective regimes shaped by nutrient availability and patterns of environmental fluctuations. Our findings specific to “ Ca. N. brevis” have broader implications, particularly in understanding the population-level responses to the changing climate and predicting its impact on biogeochemical cycles. 

ABSTRACT The field of microbial ecology, evolution, and biodiversity (EEB) is at the leading edge of understanding how microbes shape our biosphere and influence the well-being of humankind and Earth. To that end, EEB is developing new transdisciplinary tools to analyze these ecologically critical, complex microbial communities. The American Society for Microbiology’s Council on Microbial Sciences hosted a virtual retreat in 2023 to discuss the trajectory of EEB both within the Society and microbiology writ large. The retreat emphasized the interconnectedness of microbes and their outsized global influence on environmental and host health. The maximal potential impact of EEB will not be achieved without contributions from disparate fields that unite diverse technologies and data sets. In turn, this level of transdisciplinary efforts requires actively encouraging “broad” research, spanning inclusive global collaborations that incorporate both scientists and the public. Together, the American Society for Microbiology and EEB are poised to lead a paradigm shift that will result in a new era of collaboration, innovation, and societal relevance for microbiology. 

Seafloor hydrothermalism plays a critical role in fundamental interactions between geochemical and biological processes in the deep ocean. A significant number of hydrothermal vents are hypothesized to exist, but many of these remain undiscovered due in part to the difficulty of detecting hydrothermalism using standard sensors on rosettes towed in the water column or robotic platforms performing surveys. Here, we use in situ methane sensors to complement standard sensing technology for hydrothermalism discovery and compare sensors on a towed rosette and an autonomous underwater vehicle (AUV) during a 17 km long transect in the Northern Guaymas Basin in the Gulf of California. This transect spatially intersected with a known hydrothermally active venting site. These data show that methane signalled possible hydrothermal-activity 1.5–3 km laterally (100–150 m vertically) from a known vent. Methane as a signal for hydrothermalism performed similarly to standard turbidity sensors (plume detection 2.2–3.3 km from reference source), and more sensitively and clearly than temperature, salinity, and oxygen instruments which readily respond to physical mixing in background seawater. We additionally introduce change-point detection algorithms—streaming cross-correlation and regime identification—as a means of real-time hydrothermalism discovery and discuss related data supervision technologies that could be used in planning, executing, and monitoring explorative surveys for hydrothermalism.