ORCID Profile
0000-0003-4833-3106
Current Organisations
La Trobe University
,
Monash University
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Microbial ecology | Microbiology | Environmental biogeochemistry |
Publisher: Elsevier BV
Date: 04-2022
Publisher: Springer Science and Business Media LLC
Date: 04-01-2021
DOI: 10.1038/S41564-020-00811-W
Abstract: Soil microorganisms globally are thought to be sustained primarily by organic carbon sources. Certain bacteria also consume inorganic energy sources such as trace gases, but they are presumed to be rare community members, except within some oligotrophic soils. Here we combined metagenomic, biogeochemical and modelling approaches to determine how soil microbial communities meet energy and carbon needs. Analysis of 40 metagenomes and 757 derived genomes indicated that over 70% of soil bacterial taxa encode enzymes to consume inorganic energy sources. Bacteria from 19 phyla encoded enzymes to use the trace gases hydrogen and carbon monoxide as supplemental electron donors for aerobic respiration. In addition, we identified a fourth phylum (Gemmatimonadota) potentially capable of aerobic methanotrophy. Consistent with the metagenomic profiling, communities within soil profiles from erse habitats rapidly oxidized hydrogen, carbon monoxide and to a lesser extent methane below atmospheric concentrations. Thermodynamic modelling indicated that the power generated by oxidation of these three gases is sufficient to meet the maintenance needs of the bacterial cells capable of consuming them. Diverse bacteria also encode enzymes to use trace gases as electron donors to support carbon fixation. Altogether, these findings indicate that trace gas oxidation confers a major selective advantage in soil ecosystems, where availability of preferred organic substrates limits microbial growth. The observation that inorganic energy sources may sustain most soil bacteria also has broad implications for understanding atmospheric chemistry and microbial bio ersity in a changing world.
Publisher: Proceedings of the National Academy of Sciences
Date: 03-11-2021
Abstract: Diverse microbial life has been detected in the cold desert soils of Antarctica once thought to be barren. Here, we provide metagenomic, biogeochemical, and culture-based evidence that Antarctic soil microorganisms are phylogenetically and functionally distinct from those in other soils and adopt various metabolic and ecological strategies. The most abundant community members are metabolically versatile aerobes that use ubiquitous atmospheric trace gases to potentially meet energy, carbon, and, through metabolic water production, hydration needs. Lineages capable of harvesting solar energy, oxidizing edaphic inorganic substrates, or adopting symbiotic lifestyles were also identified. Altogether, these findings provide insights into microbial adaptation to extreme water and energy limitation and will inform ongoing efforts to conserve the unique bio ersity on this continent.
Publisher: Springer Science and Business Media LLC
Date: 25-05-2021
DOI: 10.1038/S41396-021-01001-0
Abstract: Desert soils harbour erse communities of aerobic bacteria despite lacking substantial organic carbon inputs from vegetation. A major question is therefore how these communities maintain their bio ersity and biomass in these resource-limiting ecosystems. Here, we investigated desert topsoils and biological soil crusts collected along an aridity gradient traversing four climatic regions (sub-humid, semi-arid, arid, and hyper-arid). Metagenomic analysis indicated these communities vary in their capacity to use sunlight, organic compounds, and inorganic compounds as energy sources. Thermoleophilia, Actinobacteria, and Acidimicrobiia were the most abundant and prevalent bacterial classes across the aridity gradient in both topsoils and biocrusts. Contrary to the classical view that these taxa are obligate organoheterotrophs, genome-resolved analysis suggested they are metabolically flexible, with the capacity to also use atmospheric H 2 to support aerobic respiration and often carbon fixation. In contrast, Cyanobacteria were patchily distributed and only abundant in certain biocrusts. Activity measurements profiled how aerobic H 2 oxidation, chemosynthetic CO 2 fixation, and photosynthesis varied with aridity. Cell-specific rates of atmospheric H 2 consumption increased 143-fold along the aridity gradient, correlating with increased abundance of high-affinity hydrogenases. Photosynthetic and chemosynthetic primary production co-occurred throughout the gradient, with photosynthesis dominant in biocrusts and chemosynthesis dominant in arid and hyper-arid soils. Altogether, these findings suggest that the major bacterial lineages inhabiting hot deserts use different strategies for energy and carbon acquisition depending on resource availability. Moreover, they highlight the previously overlooked roles of Actinobacteriota as abundant primary producers and trace gases as critical energy sources supporting productivity and resilience of desert ecosystems.
Publisher: Springer Science and Business Media LLC
Date: 10-01-2022
DOI: 10.1038/S41467-021-27769-5
Abstract: Throughout coastal Antarctica, ice shelves separate oceanic waters from sunlight by hundreds of meters of ice. Historical studies have detected activity of nitrifying microorganisms in oceanic cavities below permanent ice shelves. However, little is known about the microbial composition and pathways that mediate these activities. In this study, we profiled the microbial communities beneath the Ross Ice Shelf using a multi-omics approach. Overall, beneath-shelf microorganisms are of comparable abundance and ersity, though distinct composition, relative to those in the open meso- and bathypelagic ocean. Production of new organic carbon is likely driven by aerobic lithoautotrophic archaea and bacteria that can use ammonium, nitrite, and sulfur compounds as electron donors. Also enriched were aerobic organoheterotrophic bacteria capable of degrading complex organic carbon substrates, likely derived from in situ fixed carbon and potentially refractory organic matter laterally advected by the below-shelf waters. Altogether, these findings uncover a taxonomically distinct microbial community potentially adapted to a highly oligotrophic marine environment and suggest that ocean cavity waters are primarily chemosynthetically-driven systems.
Publisher: CSIRO Publishing
Date: 2018
DOI: 10.1071/MA18008
Abstract: Many of the world's most arid deserts harbour surprisingly erse communities of heterotrophic bacteria. These organisms persist in surface soils under extreme climatic conditions, despite lacking obvious energy inputs from phototrophic primary producers. A longstanding conundrum has been how these communities sustain enough energy to maintain their ersity and biomass. We recently helped to resolve this conundrum by demonstrating that some desert communities are structured by a minimalistic mode of chemosynthetic primary production, where atmospheric trace gases, not sunlight, serve as the main energy sources. These findings are supported by pure culture studies that suggest atmospheric trace gases are dependable energy sources for the long-term survival of dormant soil bacteria. We predict that atmospheric trace gases may be a major energy source for desert ecosystems worldwide.
Publisher: Springer Science and Business Media LLC
Date: 12-2017
DOI: 10.1038/NATURE25014
Abstract: Cultivation-independent surveys have shown that the desert soils of Antarctica harbour surprisingly rich microbial communities. Given that phototroph abundance varies across these Antarctic soils, an enduring question is what supports life in those communities with low photosynthetic capacity. Here we provide evidence that atmospheric trace gases are the primary energy sources of two Antarctic surface soil communities. We reconstructed 23 draft genomes from metagenomic reads, including genomes from the candidate bacterial phyla WPS-2 and AD3. The dominant community members encoded and expressed high-affinity hydrogenases, carbon monoxide dehydrogenases, and a RuBisCO lineage known to support chemosynthetic carbon fixation. Soil microcosms aerobically scavenged atmospheric H
Publisher: Springer Science and Business Media LLC
Date: 14-03-2019
DOI: 10.1038/S41396-019-0393-0
Abstract: Most aerobic bacteria exist in dormant states within natural environments. In these states, they endure adverse environmental conditions such as nutrient starvation by decreasing metabolic expenditure and using alternative energy sources. In this study, we investigated the energy sources that support persistence of two aerobic thermophilic strains of the environmentally widespread but understudied phylum Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class Chloroflexia) extensively remodels its respiratory chain upon entry into stationary phase due to nutrient limitation. Whereas primary dehydrogenases associated with heterotrophic respiration were downregulated, putative operons encoding enzymes involved in molecular hydrogen (H 2 ), carbon monoxide (CO), and sulfur compound oxidation were significantly upregulated. Gas chromatography and microsensor experiments showed that T. roseum aerobically respires H 2 and CO at a range of environmentally relevant concentrations to sub-atmospheric levels. Phylogenetic analysis suggests that the hydrogenases and carbon monoxide dehydrogenases mediating these processes are widely distributed in Chloroflexi genomes and have probably been horizontally acquired on more than one occasion. Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 (class Ktedonobacteria) also oxidises atmospheric H 2 and CO during persistence, though further studies are required to determine if these findings extend to mesophilic strains. This study provides axenic culture evidence that atmospheric CO supports bacterial persistence and reports the third phylum, following Actinobacteria and Acidobacteria, to be experimentally shown to mediate the biogeochemically and ecologically important process of atmospheric H 2 oxidation. This adds to the growing body of evidence that atmospheric trace gases are dependable energy sources for bacterial persistence.
Publisher: American Society for Microbiology
Date: 25-08-2020
DOI: 10.1128/MSYSTEMS.00540-20
Abstract: It is commonly thought that bacterial distributions show lower spatial variation than for multicellular organisms. In this article, we present evidence that these inferences are artifacts caused by methodological limitations. Through leveraging innovations in s ling design, sequence processing, and ersity analysis, we provide multifaceted evidence that bacterial communities in fact exhibit strong distribution patterns. This is driven by selection due to factors such as local soil characteristics. Altogether, these findings suggest that the processes underpinning ersity patterns are more unified across all domains of life than previously thought, which has broad implications for the understanding and management of soil bio ersity.
Publisher: Springer Science and Business Media LLC
Date: 06-08-2022
DOI: 10.1038/S41396-022-01298-5
Abstract: Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, bacterial primary production is supported by trace gas oxidation and the light-independent RuBisCO form IE. This study aims to determine if atmospheric chemosynthesis is widespread within Antarctic, Arctic and Tibetan cold deserts, to identify the breadth of trace gas chemosynthetic taxa and to further characterize the genetic determinants of this process. H 2 oxidation was ubiquitous, far exceeding rates reported to fulfill the maintenance needs of similarly structured edaphic microbiomes. Atmospheric chemosynthesis occurred globally, contributing significantly ( p 0.05) to carbon fixation in Antarctica and the high Arctic. Taxonomic and functional analyses were performed upon 18 cold desert metagenomes, 230 dereplicated medium-to-high-quality derived metagenome-assembled genomes (MAGs) and an additional 24,080 publicly available genomes. Hydrogenotrophic and carboxydotrophic growth markers were widespread. RuBisCO IE was discovered to co-occur alongside trace gas oxidation enzymes in representative Chloroflexota , Firmicutes , Deinococcota and Verrucomicrobiota genomes. We identify a novel group of high-affinity [NiFe]-hydrogenases, group 1m, through phylogenetics, gene structure analysis and homology modeling, and reveal substantial genetic ersity within RuBisCO form IE ( rbcL1E ), and high-affinity 1h and 1l [NiFe]-hydrogenase groups. We conclude that atmospheric chemosynthesis is a globally-distributed phenomenon, extending throughout cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental reservoirs.
Publisher: Wiley
Date: 17-08-2012
DOI: 10.1111/J.1420-9101.2012.02593.X
Abstract: Phenotypic traits that convey information about in idual identity or quality are important in animal social interactions, and the degree to which such traits are influenced by environmental variation can have profound effects on the reliability of these cues. Using inbred genetic lines of the decorated cricket, Gryllodes sigillatus, we manipulated diet quality to test how the cuticular hydrocarbon (CHC) profiles of males and females respond across two different nutritional rearing environments. There were significant differences between lines in the CHC profiles of females, but the effect of diet was not quite statistically significant. There was no significant genotype-by-environment interaction (GEI), suggesting that environmental effects on phenotypic variation in female CHCs are independent of genotype. There was, however, a significant effect of GEI for males, with changes in both signal quantity and content, suggesting that environmental effects on phenotypic expression of male CHCs are dependent on genotype. The differential response of male and female CHC expression to variation in the nutritional environment suggests that these chemical cues may be under sex-specific selection for signal reliability. Female CHCs show the characteristics of reliable cues of identity: high genetic variability, low condition dependence and a high degree of genetic determination. This supports earlier work showing that female CHCs are used in self-recognition to identify previous mates and facilitate polyandry. In contrast, male CHCs show the characteristics of reliable cues of quality: condition dependence and a relatively higher degree of environmental determination. This suggests that male CHCs are likely to function as cues of underlying quality during mate choice and/or male dominance interactions.
Publisher: American Society for Microbiology
Date: 28-04-2020
DOI: 10.1128/MSYSTEMS.00495-19
Abstract: Microbial life is surprisingly abundant and erse in global desert ecosystems. In these environments, microorganisms endure a multitude of physicochemical stresses, including low water potential, carbon and nitrogen starvation, and extreme temperatures. In this review, we summarize our current understanding of the energetic mechanisms and trophic dynamics that underpin microbial function in desert ecosystems. Accumulating evidence suggests that dormancy is a common strategy that facilitates microbial survival in response to water and carbon limitation.
Publisher: Springer Science and Business Media LLC
Date: 13-03-2021
DOI: 10.1038/S41396-021-00988-W
Abstract: Ecological theory suggests that habitat disturbance differentially influences distributions of habitat 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 physicochemical conditions. Microbial community composition and function were profiled in intertidal and subtidal sediments using 16S rRNA gene licon sequencing and metagenomics, yielding 135 metagenome-assembled genomes. Community composition and metabolic traits modestly varied with sediment depth and s ling date. Several taxa were highly abundant and prevalent in all s les, including within the orders Woeseiales and Flavobacteriales, and classified as habitat generalists genome reconstructions indicate these taxa are highly metabolically flexible facultative anaerobes and adapt to resource variability by using different electron donors and acceptors. In contrast, obligately anaerobic taxa such as sulfate reducers and candidate lineage 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 habitat generalist-associated processes of sulfide oxidation and fermentation occurred rapidly at all depths, the specialist-associated process of sulfate reduction was restricted to deeper sediments. A manipulative experiment also confirmed habitat generalists outcompete specialist taxa during simulated habitat disturbance. Together, these findings show metabolically flexible habitat generalists become dominant in highly dynamic environments, whereas metabolically constrained specialists are restricted to narrower niches. Thus, an ecological theory describing distribution patterns for macroorganisms likely extends to microorganisms. Such findings have broad ecological and biogeochemical ramifications.
Publisher: American Society for Microbiology
Date: 22-12-2020
DOI: 10.1128/MSYSTEMS.01131-20
Abstract: Desert ecosystems, spanning a third of the earth’s surface, harbor remarkably erse microbial life despite having a low potential for photosynthesis. In this work, we reveal that atmospheric hydrogen serves as a major previously overlooked energy source for a large proportion of desert bacteria. We show that both chemoheterotrophic and photoautotrophic bacteria have the potential to oxidize hydrogen across deserts s led across four continents. Whereas hydrogen oxidation was slow in native dry deserts, it increased by three orders of magnitude together with photosynthesis following hydration. This study revealed that continual harvesting of atmospheric energy sources may be a major way that desert communities adapt to long periods of water and energy deprivation, with significant ecological and biogeochemical ramifications.
Publisher: Research Square Platform LLC
Date: 13-10-2021
DOI: 10.21203/RS.3.RS-948000/V1
Abstract: Cold desert soil microbiomes thrive despite severe moisture and nutrient limitations. In Eastern Antarctic soils, hydrogen oxidising bacteria support primary production through a novel carbon fixation process reliant on the chemoautotrophy-associated RuBisCO form IE. Here, biochemical assays show that atmospheric chemosynthesis occurs globally for primary production, contributing significantly to autotrophic carbon fixation throughout arid to hyperarid deserts in Antarctica, the high Arctic, and the Tibetan Plateau. Taxonomic and functional analyses were performed on 230 dereplicated medium-to-high quality metagenome-assembled genomes (MAGs) derived from 18 cold desert metagenomes and an additional 24,080 publicly available genomes. We infer that atmospheric chemosynthetic bacteria are widespread across environmental and clinical s les, increasing our knowledge of the bacterial phyla genetically capable of atmospheric chemosynthesis to seven, with key enzymes co-occurring within MAGs from four previously unidentified phyla Chloroflexota, Firmicutes, Deinococcota and Verrucomicrobiota. We informatically identify an additional group of high-affinity hydrogenases, group 1m [NiFe]-hydrogenase using phylogenetics, gene structure analysis and homology modelling and reveal substantial new genetic ersity within RuBisCO form IE ( rbcL1E ), and high-affinity groups 1h and 1l [NiFe]-hydrogenases. Finally, we conclude that atmospheric chemosynthesis is a global phenomenon, extending throughout and beyond cold deserts, with significant implications for the global carbon cycle and bacterial survival within environmental and clinical reservoirs.
Start Date: 04-2023
End Date: 04-2026
Amount: $418,893.00
Funder: Australian Research Council
View Funded Activity