ORCID Profile
0000-0002-6627-0762
Current Organisation
Monash University
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Plant Biology | Plant Physiology | Ecosystem Function | Forestry Management and Environment
Ecosystem Assessment and Management of Forest and Woodlands Environments |
Publisher: Springer Science and Business Media LLC
Date: 09-04-2021
DOI: 10.1038/S41467-021-22333-7
Abstract: Tree stems are an important and unconstrained source of methane, yet it is uncertain whether internal microbial controls (i.e. methanotrophy) within tree bark may reduce methane emissions. Here we demonstrate that unique microbial communities dominated by methane-oxidising bacteria (MOB) dwell within bark of Melaleuca quinquenervia , a common, invasive and globally distributed lowland species. In laboratory incubations, methane-inoculated M. quinquenervia bark mediated methane consumption (up to 96.3 µmol m −2 bark d −1 ) and reveal distinct isotopic δ 13 C-CH 4 enrichment characteristic of MOB. Molecular analysis indicates unique microbial communities reside within the bark, with MOB primarily from the genus Methylomonas comprising up to 25 % of the total microbial community. Methanotroph abundance was linearly correlated to methane uptake rates (R 2 = 0.76, p = 0.006). Finally, field-based methane oxidation inhibition experiments demonstrate that bark-dwelling MOB reduce methane emissions by 36 ± 5 %. These multiple complementary lines of evidence indicate that bark-dwelling MOB represent a potentially significant methane sink, and an important frontier for further research.
Publisher: Springer Science and Business Media LLC
Date: 25-06-2022
DOI: 10.1038/S41396-022-01265-0
Abstract: Chemolithoautotrophic nitrite-oxidising bacteria (NOB) of the genus Nitrospira contribute to nitrification in erse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidiser Nitrospira moscoviensis oxidises hydrogen (H 2 ) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [ K m(app) = 32 nM]. Atmospheric H 2 oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H 2 oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Thermodynamic modelling revealed that H 2 oxidation theoretically generates higher power yield than nitrite oxidation at low substrate concentrations and significantly contributes to growth at elevated nitrite concentrations. Collectively, this study suggests atmospheric H 2 oxidation enhances the growth and survival of NOB amid variability of nitrite supply, extends the phenomenon of atmospheric H 2 oxidation to an eighth phylum (Nitrospirota), and reveals unexpected new links between the global hydrogen and nitrogen cycles. Long classified as obligate nitrite oxidisers, our findings suggest H 2 may primarily support growth and survival of certain NOB in natural environments.
Publisher: Copernicus GmbH
Date: 21-09-2020
DOI: 10.5194/BG-2020-282
Abstract: Abstract. Atmospheric trace gases such as dihydrogen (H2), carbon monoxide (CO) and methane (CH4) play important roles in microbial metabolism and biogeochemical cycles. Analysis of these gases at trace levels requires reliable storage of discrete s les of low volume. While commercial s ling vials such as Exetainers® have been tested for CH4 and other greenhouse gases, no information on reliable storage is available for H2 and CO. We show that vials sealed with butyl rubber stoppers are not suitable for storing H2 and CO due to release of these gases from rubber material. Treating butyl septa with NaOH reduced trace gas release, but contamination was still substantial, with H2 and CO concentrations in air s les increasing by a factor of 3 and 10 after 30 days of storage in conventional 12 mL Exetainers. Among the rubber materials tested, silicone showed the lowest potential for H2 and CO release. We thus propose to modify Exetainers by closing them with a silicone plug, and sealing them with a stainless steel bolt and O-ring for long-term storage. Such modified Exetainers exhibited stable concentrations of H2 and CH4 exceeding 60 days of storage at atmospheric and elevated (10 ppm) concentrations. The increase of CO was still measurable, but nine times lower than in conventional Exetainers with treated septa, and can be corrected for due to its linearity by storing a standard gas alongside the s les. The proposed modification is inexpensive, scalable and robust, and thus enables reliable storage of large numbers of low-volume gas s les from remote field locations.
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: Springer Science and Business Media LLC
Date: 24-07-2020
DOI: 10.1038/S41396-020-0722-3
Abstract: Termite mounds have recently been confirmed to mitigate approximately half of termite methane (CH 4 ) emissions, but the aerobic CH 4 oxidising bacteria (methanotrophs) responsible for this consumption have not been resolved. Here, we describe the abundance, composition and CH 4 oxidation kinetics of the methanotroph communities in the mounds of three distinct termite species s led from Northern Australia. Results from three independent methods employed show that methanotrophs are rare members of microbial communities in termite mounds, with a comparable abundance but distinct composition to those of adjoining soil s les. Across all mounds, the most abundant and prevalent methane monooxygenase sequences were affiliated with upland soil cluster α (USCα), with sequences homologous to Methylocystis and tropical upland soil cluster (TUSC) also detected. The reconstruction of a metagenome-assembled genome of a mound USCα representative highlighted the metabolic capabilities of this group of methanotrophs. The apparent Michaelis–Menten kinetics of CH 4 oxidation in mounds were estimated from in situ reaction rates. Methane affinities of the communities were in the low micromolar range, which is one to two orders of magnitude higher than those of upland soils, but significantly lower than those measured in soils with a large CH 4 source such as landfill cover soils. The rate constant of CH 4 oxidation, as well as the porosity of the mound material, were significantly positively correlated with the abundance of methanotroph communities of termite mounds. We conclude that termite-derived CH 4 emissions have selected for distinct methanotroph communities that are kinetically adapted to elevated CH 4 concentrations. However, factors other than substrate concentration appear to limit methanotroph abundance and hence these bacteria only partially mitigate termite-derived CH 4 emissions. Our results also highlight the predominant role of USCα in an environment with elevated CH 4 concentrations and suggest a higher functional ersity within this group than previously recognised.
Publisher: Copernicus GmbH
Date: 29-01-2021
Abstract: Abstract. Atmospheric trace gases such as dihydrogen (H2), carbon monoxide (CO) and methane (CH4) play important roles in microbial metabolism and biogeochemical cycles. Analysis of these gases at trace levels requires reliable storage of discrete s les of low volume. While commercial s ling vials such as Exetainers® have been tested for CH4 and other greenhouse gases, no information on reliable storage is available for H2 and CO. We show that vials sealed with butyl rubber stoppers are not suitable for storing H2 and CO due to release of these gases from rubber material. Treating butyl septa with NaOH reduced trace-gas release, but contamination was still substantial, with H2 and CO mixing ratios in air s les increasing by a factor of 3 and 10 after 30 d of storage in conventional 12 mL Exetainers. All tested materials showed a near-linear increase in H2 and CO mixing ratios, indicating a zero-order reaction and material degradation as the underlying cause. Among the rubber materials tested, silicone showed the lowest potential for H2 and CO release. We thus propose modifying Exetainers by closing them with a silicone plug to minimise contamination and sealing them with a stainless-steel bolt and O-ring as a secondary diffusion barrier for long-term storage. Such modified Exetainers exhibited stable mixing ratios of H2 and CH4 exceeding 60 d of storage at atmospheric and elevated (10 ppm) mixing ratios. The increase of CO was still measurable but was 9 times lower than in conventional Exetainers with treated septa this can be corrected for due to its linearity by storing a standard gas alongside the s les. The proposed modification is inexpensive, scalable and robust, and thus it enables reliable storage of large numbers of low-volume gas s les from remote field locations.
Publisher: American Society for Microbiology
Date: 25-06-2019
DOI: 10.1128/MSYSTEMS.00107-19
Abstract: A grand challenge in microbiology is to understand how the dormant majority lives. In natural environments, most microorganisms are not growing and instead exist in a spectrum of dormant states.
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: Copernicus GmbH
Date: 03-03-2021
DOI: 10.5194/EGUSPHERE-EGU21-1923
Abstract: & & Knowledge regarding processes, pathways and mechanisms that may moderate methane (CH& sub& & /sub& ) sink/source behaviour along the sediment - tree stem - atmosphere continuum remains incomplete. Here, we applied stable isotope analysis (& #948 & sup& & /sup& C-CH& sub& & /sub& ) to gain insights into axial CH& sub& & /sub& transport and oxidation in two common and globally distributed subtropical lowland forest species (& em& Melaleuca quinquenervia& /em& and & em& Casuarina glauca& /em& ). We found consistent trends in CH& sub& & /sub& flux (decreasing with height) and & #948 & sup& & /sup& C-CH& sub& & /sub& enrichment (increasing with height) in relation to stem height from the ground. The average lower tree stem (0-40 cm) & #948 & sup& & /sup& C-CH& sub& & /sub& of & em& M. quinquenervia& /em& and & em& C. glauca& /em& flooded forests (-53.96 & #8240 and -65.89 & #8240 ) were similar to adjacent flooded sediment CH& sub& & /sub& ebullition (-52.87 & #8240 and -62.98 & #8240 ), suggesting that CH& sub& & /sub& is produced mainly via sedimentary sources. Upper stems (81-200 cm) displayed distinct & #948 & sup& & /sup& C-CH& sub& & /sub& enrichment (& em& M. quinquenervia& /em& -44.6 & #8240 and C. glauca -46.5 & #8240 respectively) compared to lower stems. Coupled 3D photogrammetry and novel 3D measurements on & em& M. quinquenervia& /em& revealed that distinct hotspots of CH& sub& & /sub& flux and isotopic fractionation were likely due to bark anomalies where preferential pathways of gas efflux were likely enhanced. By applying a& fractionation factor (derived from previous lab based tree stem bark experiments), diel experiments revealed greater & #948 & sup& & /sup& C-CH& sub& & /sub& enrichment and higher oxidation rates in the afternoon relative to the morning. Overall, we estimate CH& sub& & /sub& oxidation rates between the lower to upper stems across both species ranged from 1 to 69 % (average 33.1 & #177 3.4 %), representing a substantial tree-associated CH& sub& & /sub& sink occurring during axial transport.& &
Publisher: Research Square Platform LLC
Date: 03-12-2020
DOI: 10.21203/RS.3.RS-119818/V1
Abstract: Tree stems are an important and unconstrained source of methane, yet it is uncertain if there are internal microbial controls (i.e. methanotrophy) within tree bark, that may reduce methane emissions. Using multiple lines of evidence, we demonstrate here that unique microbial communities dominated by methane oxidising bacteria (MOB) dwell within bark of Melaleuca quinquenervia , a common, invasive and globally distributed lowland species. Laboratory incubations of methane inoculated M. quinquenervia bark reveal methane consumption (up to 96.3 µmol m -2 bark d -1 ) and distinct isotopic δ 13 C-CH 4 enrichment characteristic of MOB. Molecular analysis indicates unique microbial communities reside within the bark, with methane-oxidising bacteria primarily from the genus Methylomonas comprising up to 25 % of the total microbial community. Methanotroph abundance was linearly correlated to methane uptake rates (R 2 = 0.76, p = 0.006). Finally, field-based methane oxidation inhibition experiments demonstrate that bark-dwelling MOB reduce methane emissions by 36 ± 5 %. These multiple, complementary lines of evidence indicate that bark-dwelling MOB represent a novel and potentially significant methane sink, and an important frontier for further research.
Publisher: Copernicus GmbH
Date: 20-06-2018
Abstract: Abstract. Termite mounds (TMs) mediate biogeochemical processes with global relevance, such as turnover of the important greenhouse gas methane (CH4). However, the complex internal and external morphology of TMs impede an accurate quantitative description. Here we present two novel field methods, photogrammetry (PG) and cross-sectional image analysis, to quantify TM external and internal mound structure of 29 TMs of three termite species. Photogrammetry was used to measure epigeal volume (VE), surface area (AE) and mound basal area (AB) by reconstructing 3-D models from digital photographs, and compared against a water-displacement method and the conventional approach of approximating TMs by simple geometric shapes. To describe TM internal structure, we introduce TM macro- and micro-porosity (θM and θμ), the volume fractions of macroscopic chambers, and microscopic pores in the wall material, respectively. Macro-porosity was estimated using image analysis of single TM cross sections, and compared against full X-ray computer tomography (CT) scans of 17 TMs. For these TMs we present complete pore fractions to assess species-specific differences in internal structure. The PG method yielded VE nearly identical to a water-displacement method, while approximation of TMs by simple geometric shapes led to errors of 4–200 %. Likewise, using PG substantially improved the accuracy of CH4 emission estimates by 10–50 %. Comprehensive CT scanning revealed that investigated TMs have species-specific ranges of θM and θμ, but similar total porosity. Image analysis of single TM cross sections produced good estimates of θM for species with thick walls and evenly distributed chambers. The new image-based methods allow rapid and accurate quantitative characterisation of TMs to answer ecological, physiological and biogeochemical questions. The PG method should be applied when measuring greenhouse-gas emissions from TMs to avoid large errors from inadequate shape approximations.
Publisher: Wiley
Date: 12-04-2021
DOI: 10.1111/NPH.17343
Abstract: Knowledge regarding mechanisms moderating methane (CH 4 ) sink/source behaviour along the soil–tree stem–atmosphere continuum remains incomplete. Here, we applied stable isotope analysis (δ 13 C‐CH 4 ) to gain insights into axial CH 4 transport and oxidation in two globally distributed subtropical lowland species ( Melaleuca quinquenervia and Casuarina glauca ). We found consistent trends in CH 4 flux (decreasing with height) and δ 13 C‐CH 4 enrichment (increasing with height) in relation to stem height from ground. The average lower tree stem δ 13 C‐CH 4 (0–40 cm) of Melaleuca and Casuarina (−53.96‰ and −65.89‰) were similar to adjacent flooded soil CH 4 ebullition (−52.87‰ and −62.98‰), suggesting that stem CH 4 is derived mainly by soil sources. Upper stems (81–200 cm) displayed distinct δ 13 C‐CH 4 enrichment ( Melaleuca −44.6‰ and Casuarina −46.5‰, respectively). Coupled 3D‐photogrammetry with novel 3D‐stem measurements revealed distinct hotspots of CH 4 flux and isotopic fractionation on Melaleuca , which were likely due to bark anomalies in which preferential pathways of gas efflux were enhanced. Diel experiments revealed greater δ 13 C‐CH 4 enrichment and higher oxidation rates in the afternoon, compared with the morning. Overall, we estimated that c . 33% of the methane was oxidised between lower and upper stems during axial transport, therefore potentially representing a globally significant, yet previously unaccounted for, methane sink.
Publisher: Cold Spring Harbor Laboratory
Date: 20-08-2021
DOI: 10.1101/2021.08.20.457082
Abstract: Chemolithoautotrophic nitrite-oxidizing bacteria (NOB) of the genus Nitrospira contribute to nitrification in erse natural environments and engineered systems. Nitrospira are thought to be well-adapted to substrate limitation owing to their high affinity for nitrite and capacity to use alternative energy sources. Here, we demonstrate that the canonical nitrite oxidizer Nitrospira moscoviensis oxidizes hydrogen (H 2 ) below atmospheric levels using a high-affinity group 2a nickel-iron hydrogenase [ K m(app) = 32 nM]. Atmospheric H 2 oxidation occurred under both nitrite-replete and nitrite-deplete conditions, suggesting low-potential electrons derived from H 2 oxidation promote nitrite-dependent growth and enable survival during nitrite limitation. Proteomic analyses confirmed the hydrogenase was abundant under both conditions and indicated extensive metabolic changes occur to reduce energy expenditure and growth under nitrite-deplete conditions. Respirometry analysis indicates the hydrogenase and nitrite oxidoreductase are bona fide components of the aerobic respiratory chain of N. moscoviensis , though they transfer electrons to distinct electron carriers in accord with the contrasting redox potentials of their substrates. Collectively, this study suggests atmospheric H 2 oxidation enhances the growth and survival of NOB in amid variability of nitrite supply. These findings also extend the phenomenon of atmospheric H 2 oxidation to a seventh phylum (Nitrospirota) and reveal unexpected new links between the global hydrogen and nitrogen cycles.
Publisher: Copernicus GmbH
Date: 21-09-2020
Start Date: 06-2021
End Date: 06-2024
Amount: $364,850.00
Funder: Australian Research Council
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