Biology subjects

Cook, P. L. M.

Publications and source records attributed to Cook, P. L. M..

8 recordsLinked to original sources

bioRxiv2025

Aridity drives global convergence of desert microbiomes and biogeochemical activities

Deserts cover a third of the worlds surface, supporting unique biomes and ecosystem services. Yet, we lack a comprehensive assessment of what defines and drives the microbial communities that dominate life in these regions. Here, we conducted a standardized field survey in contrasting cold, hot, and polar deserts across the seven continents, and observed geographically distant deserts share similar structure, function, and activities. Desert communities are dominated by genomically streamlined Actinobacteriota and Chloroflexota, and compared with non-desert soils, are significantly enriched with stress tolerance genes, mobile genetic elements, and antiviral strategies, revealing previously unknown ecological and evolutionary dynamics. Metabolically, these communities exhibit reduced capacity for carbohydrate and protein degradation, and instead are enriched for chemosynthetic carbon fixation, continuous energy harvesting using atmospheric trace gases and sunlight, and energy reserve biosynthesis. All sampled soils mediated respiration, trace gas oxidation, and carbon fixation, with detectable activity even in hyper-arid Atacama and Antarctic soils at the margins of life. Driver analyses identified aridity as the primary overriding driver of the microbial communities and biogeochemical activities. Collectively, these findings suggest that aridity selects for metabolically self-sufficient taxa capable of continuously meeting energy and carbon needs independently of vegetation-derived inputs, while enduring physicochemical stressors and potentially elevated viral pressure. These new insights are integral to forecast the future of soils amid increasing desertification. Significance statementDesert soils occupy a vast and expanding portion of Earth, yet what defines and governs their dominant microbial life remains incompletely defined. By assessing the composition, capabilities, and activities of microbial communities across deserts on all seven continents, we identify unifying signatures of life under extreme water limitation. We show microbial communities are highly self-sufficient, capable of acquiring energy and carbon even where plant inputs are minimal. This planetary-scale understanding of the desert microbiome has important ramifications for forecasting potential shifts of microbial communities and the services they provide as desertification intensifies.

microbiology↗

bioRxiv2025

Bark-associated diazotroph communities are a cryptic source of nitrogen in forests

Nitrogen is an essential nutrient limiting forest productivity. Plants cannot access atmospheric N2 directly and rely on diazotrophic bacteria to fix nitrogen into bioavailable forms such as ammonium. Within forests, biological nitrogen fixation (BNF) occurs primarily in soils and root nodules. However it is unclear whether the extensive microbial communities recently discovered in tree bark can also fix nitrogen. Here we combine field measurements, metagenomic profiling, and biogeochemical assays to show that bark-dwelling diazotroph communities are abundant and active across diverse tree species. Bark from eight Australian tree species showed exceptionally high C:N ratios and depleted nitrogen stable isotope signatures ({delta}15N) consistent with locally fixed nitrogen, suggesting strong selection for diazotrophs. Consistently, bark microbial communities harbour phylogenetically and physiologically diverse diazotrophs, averaging [~]1012 cells m-2 and in higher relative abundance than underlying soils. Canonical and alternative nitrogenases were detected across eight bacterial phyla, primarily bark-adapted Alphaproteobacteria, Acidobacteriota, and Verrucomicrobiota, with strong signatures of purifying selection. Stable isotope labelling experiments demonstrated that bark-dwelling diazotrophs fix nitrogen at rates varying with tree species and habitat. In line with the presence of methane-oxidising diazotrophs, BNF was strongly stimulated by methane addition and suppressed by methanotroph inhibitors. Initial upscaling suggests bark-associated nitrogen fixation contributes up to 3.8 Tg N yr-1 globally ([~]6% of natural terrestrial BNF), with further studies required to constrain this budget and its contribution to tree nitrogen demands. Altogether, this discovery of substantial above-ground nitrogen inputs revises our understanding of forest nutrient cycles and redefines the functional scope of the caulosphere.

microbiology↗

bioRxiv2025

Chemosynthesis enables microbial communities to flourish in a marine cave ecosystem

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 sedimentary microorganisms within 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 its 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.

ecology↗

bioRxiv2025

Chemosynthesis enhances carbon fixation in an active microbialite ecosystem

Microbialites--carbonate structures formed under the influence of microbial action-- are the earliest macroscopic evidence of life. For three billion years, the microbial mat communities responsible for these structures fundamentally shaped Earths biogeochemical cycles. In photosynthetic microbial communities, light energy ultimately drives primary production and the ensuing cascade of daisy-chained metabolisms. However, reduced compounds such as trace gases and those released as metabolic byproducts in deeper, anoxic regions of the mat, could also fuel chemosynthetic processes. Here, we investigated the intricate metabolic synergies that sustain microbialite community nutrient webs. We recovered 331 genomes spanning 40 bacterial and archaeal phyla, revealing a staggering diversity fuelled by the biogeochemistry of these ecosystems. While phototrophy is an important metabolism encoded by 17% of the genomes, over half encode enzymes to harness energy from reduced compounds and 12% co-encode carbon fixation pathways, using sulfide and hydrogen as major electron donors. Consistent with these genomic predictions, we experimentally demonstrated that microbialite communities oxidise ferrous iron, ammonia, sulfide and gas substrates aerobically and anaerobically. Furthermore, carbon isotopic assays revealed that diverse chemosynthetic pathways contribute significantly to carbon fixation and ecosystem organic matter production alongside photosynthesis. Chemosynthesis in microbialite communities represents a complex interplay of metabolic synergies and continuous nutrient cycling, which decouples community carbon fixation from the diurnal cycle. As a result, this process mitigates the loss of organic carbon from respiration, enhancing the net productivity of these highly efficient ecosystems. SignificanceMicrobialite ecosystems are among the most ancient on Earth, having dominated the biosphere for over three billion years and persisting into the present. They serve as critical models for studying past and present Earth-biosphere interactions. In this study, we challenge the paradigm that photosynthesis is the main driver of microbialite primary productivity, emphasizing the fundamental role of chemosynthesis in the global element cycle both in modern extreme environments and throughout Earths history. Altogether, our findings provide novel insight into these unique microbial ecosystems, which may have functioned as hotspots for metabolic innovation over geological time.

microbiology↗

bioRxiv2024

Microbial aerotrophy enables continuous primary production in diverse cave ecosystems

Most aerated cave ecosystems are assumed to be oligotrophic given they receive minimal inputs of light energy. Diverse microorganisms have nevertheless been detected within caves, though it remains unclear what strategies enable them to meet their energy and carbon needs. Here we determined the processes and mediators of primary production in aerated limestone and basalt caves through paired metagenomic and biogeochemical profiling. Based on 1458 metagenome-assembled genomes, over half of microbial cells in caves encode enzymes to use atmospheric trace gases as energy and carbon sources. The most abundant microbes in these systems are chemosynthetic primary producers, notably the novel gammaproteobacterial methanotrophic order Ca. Methylocavales and two uncultivated actinobacterial genera predicted to grow on atmospheric hydrogen, carbon dioxide, and carbon monoxide. In situ and ex situ biogeochemical and isotopic measurements consistently confirmed that these gases are rapidly consumed at rates sufficient to meet community-wide energy needs and drive continual primary production. Conventional chemolithoautotrophs, which use trace lithic compounds such as ammonium and sulfide, are also enriched and active alongside these trace gas scavengers. These results indicate that caves are unique in both their microbial composition and the biogeochemical processes that sustain them. Based on these findings, we propose caves are the first known ecosystems where atmospheric trace gases primarily sustain growth rather than survival and define this process as aerotrophy. Cave aerotrophy may be a hidden process supporting global biogeochemistry.

microbiology↗

bioRxiv2022

Molecular hydrogen is an overlooked energy source for marine bacteria

Molecular hydrogen (H2) and carbon monoxide (CO) are supersaturated in seawater relative to the atmosphere and hence are readily accessible energy sources for marine microbial communities. Yet while marine CO oxidation is well-described, it is unknown whether seawater communities consume H2. Here we integrated genome-resolved metagenomics, biogeochemistry, thermodynamic modelling, and culture-based analysis to profile H2 and CO oxidation by marine bacteria. Based on analysis of 14 surface water samples, collected from three locations spanning tropical to subantarctic fronts, three uptake hydrogenase classes are prevalent in seawater and encoded by major marine families such as Rhodobacteraceae, Flavobacteriaceae, and Sphingomonadaceae. However, they are less abundant and widespread than carbon monoxide dehydrogenases. Consistently, microbial communities in surface waters slowly consumed H2 and rapidly consumed CO at environmentally relevant concentrations, with H2 oxidation most active in subantarctic waters. The cell-specific power from these processes exceed bacterial maintenance requirements and, for H2, can likely sustain growth of bacteria with low energy requirements. Concordantly, we show that the polar ultramicrobacterium Sphingopyxis alaskensis grows mixotrophically on H2 by expressing a group 2a [NiFe]-hydrogenase, providing the first demonstration of atmospheric H2 oxidation by a marine bacterium. Based on TARA Oceans metagenomes, genes for trace gas oxidation are globally distributed and are fourfold more abundant in deep compared to surface waters, highlighting that trace gases are important energy sources especially in energy-limited waters. Altogether, these findings show H2 is a significant energy source for marine communities and suggest that trace gases influence the ecology and biogeochemistry of oceans globally.

microbiology↗

bioRxiv2020

Efficient long-range conduction in cable bacteria through nickel protein wires

Filamentous cable bacteria display unrivalled long-range electron transport, generating electrical currents over centimeter distances through a highly ordered network of fibers embedded in their cell envelope. The conductivity of these periplasmic wires is exceptionally high for a biological material, but their chemical structure and underlying electron transport mechanism remain unresolved. Here, we combine high-resolution microscopy, spectroscopy, and chemical imaging on individual cable bacterium filaments to demonstrate that the periplasmic wires consist of a conductive protein core surrounded by an insulating shell layer. The core proteins contain a sulfur-ligated nickel cofactor, and conductivity decreases when nickel is oxidized or selectively removed. The involvement of nickel as the active metal in biological conduction is remarkable, and suggests a hitherto unknown form of electron transport that enables efficient conduction in centimeter-long protein structures.

microbiology↗

bioRxiv2020

Metabolic flexibility allows generalist bacteria to become dominant in a frequently disturbed ecosystem

Ecological theory suggests that habitat disturbance differentially influences distributions of generalist and specialist species. While well-established for macroorganisms, this theory has rarely been explored for microorganisms. Here we tested these principles in permeable (sandy) sediments, ecosystems with much spatiotemporal variation in resource availability and other conditions. Microbial community composition and function was profiled in intertidal and subtidal sediments using 16S amplicon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Microbial abundance and composition significantly differed with sediment depth and, to a lesser extent, sampling date. Several generalist taxa were highly abundant and prevalent in all samples, including within orders Woeseiales and Flavobacteriales; genome reconstructions indicate these facultatively anaerobic taxa are highly metabolically flexible and adapt to fluctuations in resource availability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers (Desulfobacterales, Desulfobulbales) and proposed candidate phylum MBNT15 were less abundant overall and only thrived in more stable deeper sediments. We substantiated these findings by measuring three metabolic processes in these sediments; whereas the generalist-associated processes of sulfide oxidation and hydrogenogenic fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. In addition, a manipulative experiment confirmed generalists outcompete specialist taxa during simulated habitat disturbance. Altogether, these findings suggest that metabolically flexible taxa become dominant in these highly dynamic environments, whereas metabolic specialism restricts bacteria to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.

microbiology↗