Abstract. Methane emissions from coastal sediments are increasingly influenced by ecological change, including eutrophication-driven seaweed blooms and efforts to restore coastal vegetation. Yet the pathways and variability of methane production in these environments remain poorly constrained. Here, we compared methane production from three seaweeds (Ulva, red filamentous algae, and kelp) and three coastal plants (mangrove leaves, saltmarsh plants, and seagrass) in sands from Port Phillip Bay, Australia. To identify potential predictive precursors, we quantified key methylated osmolytes (dimethyl sulfoniopropionate (DMSP), choline, trimethylamine (TMA), trimethylamine N-oxide (TMAO)), that serve as methanogenic substrates. Methane production from seaweeds was strongly correlated with osmolyte content, whereas coastal plants, particularly mangrove leaves, stimulated methane production despite low osmolyte levels, likely via decomposition pathways generating methanol. These findings broaden the understanding of organic matter sources fueling methanogenesis in coastal sediments and highlight an overlooked contribution of both seaweeds and plants to coastal methane cycling.
The atmosphere could be one of Earth’s largest and most interconnected ecosystems. It is an environment characterized by low temperatures, low nutrient availability, aridity, and high ultraviolet radiation. Nevertheless, research in cold, arid and oligotrophic extreme environments have demonstrated that the conditions of the atmosphere are within the boundaries currently considered to support microbial life. Moreover, certain microorganisms are capable of gaining energy by oxidizing atmospheric gasses (hydrogen (H2), carbon monoxide (CO) and methane (CH4)) at trace concentrations. Measurement and experimental investigations of the atmospheric microbiome (the aeromicrobiome) are extremely challenging due to the compounding difficulties of low biomass samples, contamination issues, and lack of standardized sampling procedures. Numerical modelling can advance aeromicrobiology research by providing a complementary means to evaluate the habitability of the atmosphere and the potential activity of atmospheric microorganisms. We developed a theoretical framework combining the state-of-the-art knowledge of potential atmospheric-dwelling microorganisms, thermodynamic principles, and global climate and atmospheric gas composition data from MERRA2 (Modern-Era Retrospective analysis for Research and Applications, v2) and CAMS (Copernicus Atmosphere Monitoring Service). Our modelling analysis demonstrates that hydrogen oxidation, carbon monoxide oxidation, and methane oxidation are energy yielding catabolisms (ΔGr < 0, i.e. thermodynamically feasible) under atmospheric conditions, throughout the entire troposphere, all year round. It is therefore possible that these catabolisms are a viable source of energy to microorganisms in the atmosphere. We also reveal spatially and temporal energetic ‘hot spots’ where catabolic energy yield is greater, due to localized atmospheric gas concentrations and temperatures. In addition to supplying energy, atmospheric methane oxidation and hydrogen oxidation generate water as a catabolic byproduct, potentially alleviating limitations to microbial survival and activity that are imposed by the extreme aridity of the atmosphere. Theoretical modelling can accelerate aerobiology research by generating theory-informed hypotheses about which microbial cohorts are more probable to be metabolically active in the Earth’s atmosphere and guiding experimental research to where and how we may find and study them.
Chemosynthesis, an ancient metabolism that uses chemical compounds for energy and biomass generation, occurs across the ocean. Although chemosynthesis typically plays a subsidiary role to photosynthesis in the euphotic ocean, it is unclear whether it plays a more important role in aphotic habitats within this zone. Here, we compared the composition, function, and activity of microorganisms colonising the sediment of a marine cave at mesophotic depth, across a transect from the entrance to the interior. Microbes thrived throughout this ecosystem, with interior communities having higher diversity than those at the entrance. Analysis of 132 species-level bacterial, archaeal, and eukaryotic metagenome-assembled genomes revealed niche partitioning of habitat generalists distributed along the cave, alongside specialists enriched across the entrance and interior environments. Photosynthetic microbes and photosystem genes declined in the inner cave, concomitant with enrichment of chemosynthetic lineages capable of using inorganic compounds such as ammonium, sulfide, carbon monoxide, and hydrogen. Biogeochemical assays confirmed that the cave communities consume these compounds and fix carbon dioxide through chemosynthesis, with inner communities mediating higher cellular rates. Together, these findings suggest that the persistent darkness and low hydrodynamic disruption in marine cave sediments create conditions for metabolically diverse communities to thrive, sustained by recycling of inorganic compounds, as well as endogenous and lateral organic matter inputs. Thus, chemosynthesis can sustain rich microbial ecosystems even within the traditionally photosynthetically dominated euphotic zone.
Antarctica’s compositionally and functionally unusual biodiversity is typically neglected in global biodiversity analyses, and ecological theory is rarely applied in the Antarctic context. These omissions mean that predictions of the future of Antarctic biodiversity under global change are weakly guided by mechanistic understanding. In this Perspective, we provide an overview of Antarctica’s biodiversity and key changes in its terrestrial environment and then discuss how five central ecological processes (abiotic filtering, dispersal, adaptation, biotic interactions and stochasticity) are affecting biodiversity on the continent. On the basis of the evidence supporting each of these processes, we establish five non-exclusive hypotheses for terrestrial Antarctic biodiversity outcomes under global change: constrained, dynamic, disordered, diversifying and interactive. Available evidence best supports the constrained hypothesis, in which abiotic conditions will probably remain a dominant constraint to fitness, even in warmer, wetter conditions. The five biodiversity outcomes we articulate provide theory-driven, testable hypotheses for Antarctic biodiversity and identify priority knowledge gaps to reduce uncertainty about its future. Antarctica has a unique environment and geographic isolation that affect its biodiversity patterns. In this Perspective, the authors examine how five key ecological processes shape Antarctica’s biodiversity and use this information to establish predictions for future change in the region.
Dimethyl sulfide (DMS) and dimethyl sulfoxide (DMSO) have important microbial-driven roles in global nutrient cycling, chemotaxis and/or climate regulation. Microbial DMSO and DMS assimilation were thought to require their enzymatic reduction to methanethiol. However, reactive oxygen species were recently shown to mediate methane production from DMS and DMSO. Here, we show that this oxidative mechanism can sustain microbial growth without the need for enzymes to directly reduce DMS or oxidize DMSO. Both, light and heat were effective geochemical drivers of this mechanism that yielded methanesulfonic acid and sulfite, and which mimicked the stepwise oxidation of DMSO by monooxygenases that only enzymatically enhance this oxidation reaction. Furthermore, we demonstrated intracellular DMSO degradation, in which sulfur and the simultaneously released carbon were both utilized by microbes. This study emphasizes that metabolic pathways are not necessarily enzyme-driven, with putatively ancient, non-enzymatic reaction networks taking place at a transition between geochemistry and biochemistry.
Extreme anoxic environments are hotspots of sulfur cycling and harbor numerous novel uncharacterized microbial lineages. Although the phylum Joyebacterota was recently proposed, its internal phylogenetic architecture and evolutionary adaptations remain poorly understood. Here, we significantly expand the genomic diversity and metabolic framework of this phylum by integrating recovered metagenome-assembled genomes, and propose a novel genus, Cavimicrobium. Phylogenomic analysis placed Cavimicrobium as a distinct clade and further divided into four species-level subgroups associated with diverse anoxic sources, including sediments from the Salton Sea, the Eastern Gotland Basin, and the anoxic waters of the Sansha Yongle Blue Hole (SYBH). Unlike previous broad surveys, our study revealed that this lineage evolved from a facultatively anaerobic ancestor and underwent adaptive gene gain and loss through phylogenetic reconstruction. Genomic evidence suggested that this lineage harbored a previously overlooked anaerobic sulfite reduction (asrABC) pathway that likely mediating thiosulfate uptake and conversion to sulfite and sulfide. Notably, Cavimicrobium was particularly abundant in the anoxic waters of SYBH, comprising up to one-third of the bacterial community in particle-associated fraction below 100 m, where it is likely a major contributor to sulfide accumulation. Analysis of MAGs and global amplicon datasets revealed that Cavimicrobium is widespread across anoxic environments, comprising up to 0.32% of the bacterial community in 354 200 publicly available 16S rRNA gene amplicon samples. Together, these findings reveal a new lineage dominant in certain anoxic environments where they are likely important mediators of sulfur cycling, and broaden our understanding of biogeochemical potential of Joyebacterota.
Nearly one-fifth of global emissions of the potent greenhouse gas nitrous oxide (N2O) originate from the ocean, particularly from nutrient-polluted coastal regions. Permeable (sandy) sediments, which cover half of the continental shelf worldwide, are potential sources of N2O due to increasing nutrient inputs from urbanization and agriculture. Yet, the microbial processes determining N2O emissions in these dynamic and unique ecosystems remain understudied. Here, we combined environmental measurements, bacterial cultivation, and genomic analyses to understand the microbes and processes controlling N2O cycling in permeable sediments from Port Phillip Bay (Australia). We established a genomic resource comprising 249 metagenome-assembled genomes and 95 new isolate genomes. Genome-based metabolic reconstructions and culture-based gas measurements revealed that diverse bacteria in these sediments produce N2O through incomplete denitrification pathways. However, these bacteria co-occurred with highly abundant clade II N2O-reducing bacteria from the Flavobacteriaceae family. Kinetic profiling showed that both clade II nosZ flavobacterial isolates and whole sand communities exhibited a low apparent affinity for N2O under the tested experimental conditions, expanding the currently limited kinetic data available for N2O reducing microorganisms from coastal permeable sediments, including flavobacterial clade II N2O reducers. Collectively, these findings indicate that abundant N₂O reducing communities can substantially consume N2O within permeable sediments, thus limiting N2O accumulation despite active N2O production. Together with previous hydrodynamic models predicting low N2O release from permeable sediments, our results highlight the important role of specialized microbial communities in regulating N2O cycling under increasing nutrient pollution.
Antarctic soils represent one of the most extreme environments for microbial life on Earth, yet they harbor heterogeneous and diverse microbial communities. Biologists have long hypothesized that Antarctic microorganisms are unique from those found on other continents due to the extreme geographic isolation and the cold, dry, and challenging conditions typical of Antarctica. To test this hypothesis, we focused on a cosmopolitan bacterial genus, Arthrobacter, that is widely distributed across global soils. We first profiled a global metagenomic dataset from both Antarctic and non-Antarctic surface soils to quantify the distributions of Arthrobacter strains. Despite high strain-level diversity, 90% of the strains found in the Antarctic soils were only found on the continent. We then used cultivation-based phenotypic analyses and strain-level genomic comparisons to assess how Antarctic strains and non-Antarctic strains differ in their traits and environmental preferences. Not only did we find evidence of endemism, but Antarctic Arthrobacter also have genomic characteristics and environmental tolerances that suggest they are uniquely adapted to Antarctic conditions.
Abstract Molecular hydrogen (H 2 ) and hydrogen sulfide (H 2 S) are central gut metabolites that shape microbial metabolism and affect host health. In Crohn’s disease (CD), the shift in microbiota composition (‘dysbiosis’) is associated with intestinal accumulation of these gases, but the responsible microbes remain poorly resolved. Here, we analysed 4,644 bacterial and archaeal species-level genomes from the Unified Human Gastrointestinal Genome Collection to identify H 2 -cycling microbes, assessed their prevalence in ca. 1,700 stool metagenomes from healthy and diseased individuals, and validated their activity using culture-based incubations of stool isolates and biopsy samples. Approximately half of all species encoded H 2 -producing abilities, with acetate- and propionate-forming fermenters such as Phocaeicola and Bacteroides dominating healthy cohorts, whereas comparatively few taxa, including Escherichia and Megamonas , encoded H 2 consuming abilities. In CD, H 2 producers became more abundant but less diverse, favouring species with multiple H 2 -evolving hydrogenases and more fermentation routes, especially Clostridium and Enterocloster species. Consistently, isolates enriched in CD produced H 2 faster and at higher concentrations than health-associated isolates. Increased H 2 S-producing capacity in CD was driven mainly by these H 2 -producing fermenters carrying anaerobic sulfite reductases (Asr), rather than sulfate-reducing bacteria, and was supported by elevated H 2 S production in Asr-positive isolates, likely providing an additional electron sink. These findings provide a species-resolved view of gut gas metabolism and implicate metabolically flexible fermenters in excessive gas and sulfide production in gut disorders.
Diverse microorganisms couple the oxidation of carbon monoxide gas (CO) to the reduction of protons, producing hydrogen gas (H2) using nickel-containing CO dehydrogenase/energy-converting hydrogenase (Ni-CODH/ECH). Although this process yields one of the lowest free-energy gains in biology, its physiological role at environmentally relevant CO levels remains unresolved. Here, we show that Ni-CODH/ECH functions as a survival-oriented energy conservation system that enables heterotrophic facultative anaerobes to survive electron acceptor limitation, rather than primarily supporting growth or CO detoxification. Analysis of 387 genomes of Anoxybacillaceae species revealed that Ni-CODH/ECH had a patchy distribution and, with one exception, was mutually exclusive with the oxygen-tolerant molybdenum-containing CODH, suggesting ecological specialization. Culture experiments using three isolates (Parageobacillus sp. G301, P. thermoglucosidasius NBRC 107763, and Thermolongibacillus altinsuensis B1-1) demonstrated that CO-dependent proton respiration is activated during stationary phase when exogenous electron acceptors are limiting, maintaining cell density under 25% CO, whereas no effect was observed in a Ni-CODH knockout (ΔcooCSF) strain. RNA-seq analysis of Parageobacillus sp. G301 under twelve conditions revealed that Ni-CODH/ECH genes are highly expressed (top 0.2%-1.9% of all genes) under electron acceptor-free conditions, independent of CO presence, under the predicted control of the redox-dependent transcriptional repressor Rex. ΔcooCSF cultures accumulated more CO than the wild-type (WT), suggesting trace CO scavenging by the WT. Together, our results redefine Ni-CODH/ECH as a redox-regulated auxiliary energy-conservation strategy that supports survival and maintenance in anaerobic energy-limited environments using two ubiquitous substrates. This work extends the carboxydovore paradigm of trace gas-based survival from aerobic to spatiotemporally variable anaerobic environments.
The atmosphere is increasingly recognised as a major energy source supporting life. Numerous microbes, termed aerotrophs, use high-affinity enzymes to harvest energy from atmospheric hydrogen, carbon monoxide, and methane. This metabolism shapes atmospheric chemistry and sustains biodiversity across diverse ecosystems. This primer summarises the basis, roles, and significance of aerotrophy.
Recent studies suggest that microbes inhabit tree bark, yet little is known about their identities, functions, and environmental roles. Here we reveal, through gene-centric and genome-resolved metagenomics, that the bark of eight common Australian tree species hosts abundant and specialized microbial communities. The predominant bacteria are hydrogen-cycling facultative anaerobes adapted to dynamic redox and substrate conditions. Furthermore, bark-associated methanotrophs are abundant and can coexist with hydrogenotrophic methanogens. Microcosm experiments showed that bark microorganisms aerobically consume methane, hydrogen, and carbon monoxide at in planta concentrations and produce these gases under anoxia. Combined with in situ field measurements, we show that tree-dwelling microbiota metabolize multiple climate-active gases at marked rates within tree stems, highlighting a potentially substantial role in global atmospheric cycles.
In soil ecosystems, aerobic bacteria survive oxygen deprivation (hypoxia) by entering nonreplicative persistent states. In contrast to the well-studied metabolism of obligate and facultative anaerobes, little is known about how obligately aerobic bacteria adapt their metabolism to stay viable during hypoxia. The model obligate aerobe Mycobacterium smegmatis maintains redox homeostasis during hypoxia by mediating fermentative hydrogen production. However, the fate of organic carbon during fermentation is unresolved. Here we systematically profiled the metabolism of M. smegmatis during aerobic growth, hypoxic persistence, and the transition between these states. By integrating a differentially 13C-labeled glucose isotopologue assay with paired metabolomics and proteomics, we observed M. smegmatis rerouted central carbon metabolism through the pentose phosphate pathway and/or Entner-Doudoroff pathways during hypoxia, while excreting high levels of hydrogen and acetate. Lipid and cryoelectron tomography analyses suggest M. smegmatis also stores carbon as glycerides in lipid droplets during hypoxia, which serve as a major reductant sink. Gene knockouts and knockdowns revealed that, while M. smegmatis depends on its hydrogen-producing hydrogenase for hypoxic survival, it can compensate for the disruption of acetate production and glyceride synthesis by producing and excreting other organic acids. We confirmed through an extensive genomic survey and biogeochemical measurements that diverse aerobic soil bacteria can store organic carbon and mediate fermentation during hypoxia. Altogether, this hybrid fermentative metabolism likely provides a competitive advantage in soils and other resource-variable environments by enabling bacteria, such as M. smegmatis, to simultaneously dispose excess reductant and maintain carbon stores during hypoxia.
Abstract Phenotypically agnostic screens for positive selection in pathogen populations provide a means of pinpointing genes and regulatory regions involved in adaptation to the local environment or host population. We screened a large (n = 2506) collection of Vietnamese Mycobacterium tuberculosis (Mtb) isolates, finding targets of selection to be lineage-specific, and encompass diverse functions, including dormancy (Rv0080), zinc homeostasis (zur), and virulence (ESX-1 structure). Extending our screen to the wider Mtb complex (MTBC) phylogeny demonstrated Rv0080 to display an extraordinarily dynamic evolutionary history, acquiring premature stop codons or putative functional mutations on branches upstream of 8 of the 10 human-adapted lineages, and undergoing positive selection in the remaining 2. Lineage 1, which is one of two such lineages retaining the ancestral Rv0080 sequence, displays a rate of selection for this gene (dN/dS=9.37) exceeding any other in the Mtb genome, save a transcription factor linked to its expression (Rv0042c; dN/dS=11.02). Deletion of Rv0080’s M. smegmatis orthologue confers a survival advantage in hypoxic conditions, as does the evolution of nonsense or missense mutations on an ancestral Rv0080 background. We show the dormancy survival regulon experienced recurrent episodes of reductive evolution across the MTBC phylogeny, illuminating a novel mechanism via which it adapted to human populations.
Cellular respiration depends on transferring electrons to hydrophobic quinones in membrane bilayers, meaning bioenergetic capacity is constrained by available membrane surface area. While Gram-negative bacteria expand this capacity through internal membrane invaginations and eukaryotes use membrane-bound organelles, whether Gram-positive bacteria have alternative capacity-generating mechanisms is unknown. Here we show that Bacillus subtilis forms a quinone-transporting pseudomembrane composed of filaments of the NADH dehydrogenase Ndh and the quinone-transporting protein Ncp. Cryo-EM, lipidomics and molecular dynamics reveal that Ndh and Ncp co-assemble with lipids into a 4:4 stoichiometric complex with a solvent-excluded hydrophobic lumen containing phospholipids, which sequesters quinones. These complexes further assemble into filaments, linking chambers into a continuous conduit that amplifies quinone reduction. Phylogenetic analysis suggests that this capacity is widespread in Bacillota. Quinone-transporting filaments thus reveal a strategy to expand the quinone pool and bioenergetic capacity while occupying minimal membrane space.
Asgard archaea were pivotal in the origin of complex cellular life1. Heimdallarchaeia (a class within the phylum Asgardarchaeota) are inferred to be the closest relatives of eukaryotes. Limited sampling of these archaea constrains our understanding of their ecology and evolution2,3, including their role in eukaryogenesis. Here we use massive DNA sequencing of marine sediments to obtain 404 Asgardarchaeota metagenome-assembled genomes, including 136 new Heimdallarchaeia and several novel lineages. Analyses of their global distribution revealed they are widespread in marine environments, and many are enriched in variably oxygenated coastal sediments. Detailed metabolic reconstructions and structural predictions suggest that Heimdallarchaeia form metabolic guilds that are distinct from other Asgardarchaeota. These archaea encode hallmark proteins of an aerobic lifestyle, including electron transport chain complex (IV), haem biosynthesis and reactive oxygen species detoxification. Heimdallarchaeia also encode novel clades of respiratory membrane-bound hydrogenases with additional Complex I-like subunits, which potentially increase proton-motive force generation and ATP synthesis. Thus, we propose an updated Heimdallarchaeia-centric model of eukaryogenesis in which hydrogen production and aerobic respiration may have been present in the Asgard-eukaryotic ancestor. This expanded catalogue of Asgard archaeal genomic diversity suggests that bioenergetic factors influenced eukaryogenesis and constitutes a valuable resource for investigations into the origins and evolution of cellular complexity.
Abstract Cellular respiration depends on transferring electrons to hydrophobic quinones in membrane bilayers, constraining capacity to available surface area. Expanding this capacity is thought to have driven cellular complexity and eukaryogenesis, with Gram-negative bacteria evolving internal invaginations and eukaryotes using membrane-bound organelles. Whether Gram-positive bacteria, which lack such membranes, evolved alternatives was unknown. Here, we show that Bacillus subtilis forms a quinone-transporting pseudomembrane composed of filaments of the NADH dehydrogenase Ndh and the quinone-transporting protein Ncp. Cryo-EM, lipidomics, and molecular dynamics reveal that Ndh and Ncp co-assemble with phospholipids into a complex containing a solvent-excluded hydrophobic lumen that sequesters quinones. These complexes further assemble into filaments, linking chambers into a continuous conduit that amplifies quinone reduction while occupying minimal membrane space. Phylogenetic analysis suggests this recent innovation is widespread in Bacillota. Quinone-transporting filaments thus reveal a third strategy for overcoming surface-area limits and provide principles for engineering synthetic energy systems.
Microbial Solutions for a Changing World was an inaugural international conference hosted at Monash University, Melbourne, and presented by Applied Microbiology International. The meeting brought together researchers from across the Asia-Pacific region to examine how microbiological research informs responses to climate-related challenges across environmental, health, and applied contexts. Recognizing the central role of microorganisms in regulating greenhouse gas fluxes, shaping disease dynamics, and underpinning ecosystem function, it provided a forum for focused exchange at the intersection of microbiology and climate research. The programme was organized around three thematic areas: greenhouse gas cycling and mitigation, health impacts and pathogen control, and environmental impacts and ecosystem restoration. Plenary lectures and contributed presentations addressed microbial processes operating across managed, natural, and extreme environments, alongside discussion of how microbiological insight can inform mitigation, disease management, and restoration strategies under changing environmental conditions. Early-career researchers were placed at the centre of the programme, with structured activities aimed at supporting interaction and collaboration. By convening researchers working across diverse sub-disciplines, the conference highlighted common challenges and opportunities in aligning microbiology with climate response efforts. Microbial Solutions for a Changing World demonstrated the value of dedicated forums for advancing sustainable microbiology within the Asia-Pacific region and beyond.