Molecular Hydrogen, a Neglected Key Driver of Soil Biogeochemical Processes

Piché-Choquette, Sarah; Constant, Philippe

doi:10.1128/aem.02418-18

Cited by 55 publications

(49 citation statements)

References 203 publications

(238 reference statements)

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“…Huc is expressed by M. smegmatis during the transition from growth to persistence, allowing cells to grow mixotrophically on atmospheric H 2 and, where available, higher concentrations produced through abiotic or biotic processes (e.g. fermentation, nitrogen fixation) (39). Subsequently, as cells commit to persistence due to carbon starvation, Hhy is expressed and supplies energy from atmospheric H 2 to meet maintenance needs.…”

Section: Resultsmentioning

confidence: 99%

Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence

Cordero

Grinter

Hards

et al. 2019

Preprint

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21Aerobic soil bacteria metabolize atmospheric hydrogen (H2) to persist when nutrient 22 sources are limited. This process is the primary sink in the global H2 cycle and supports 23 the productivity of microbes in oligotrophic environments. To mediate this function, 24 bacteria possess [NiFe]-hydrogenases capable of oxidising H2 to subatmospheric 25 concentrations. The soil saprophyte Mycobacterium smegmatis has two such [NiFe]-26 hydrogenases, designated Huc and Hhy, which belong to different phylogenetic 27 subgroups. Huc and Hhy exhibit similar characteristics: both are oxygen-tolerant, 28 oxidise H2 to subatmospheric concentrations, and enhance survival during hypoxia 29 and carbon limitation. These shared characteristics pose the question: Why does M. 30 smegmatis require two hydrogenases mediating a seemingly similar function? In this 31 work we resolve this question by showing that Huc and Hhy are differentially 32 expressed, localised, and integrated into the respiratory chain. Huc is active in late 33 exponential and early stationary phase, supporting energy conservation during 34 mixotrophic growth and the transition into dormancy. In contrast, Hhy is most active 35 during long-term persistence, providing energy for maintenance processes when 36 carbon sources are depleted. We show that Huc and Hhy are obligately linked to the 37 aerobic respiratory chain via the menaquinone pool and are differentially affected by 38 respiratory uncouplers. Consistent with their distinct expression profiles, Huc and Hhy 39 interact differentially with the terminal oxidases of the respiratory chain. Huc 40 exclusively donates electrons to, and possibly physically associates with, the proton 41 pumping cytochrome bcc-aa3 supercomplex. In contrast, the more promiscuous Hhy 42 can also provide electrons to the cytochrome bd oxidase complex. These data 43 demonstrate that, despite their similar characteristics, Huc and Hhy perform distinct 44 functions during mycobacterial growth and survival.45 46 48 the past decade, research by a number of groups has revealed that this net H2 49 consumption is mediated by aerobic soil bacteria (3-8). Based on this work, it has 50 been established that gas-scavenging bacteria are the major sink in the global H2 cycle, 51 responsible for the net consumption of approximately 70 million tonnes of H2 each 52year and 80 percent of total atmospheric H2 consumed (6,(9)(10)(11). In addition to its 53 biogeochemical importance, it is increasingly realised that atmospheric H2 oxidation is 54 important for supporting the productivity and biodiversity of soil ecosystems (12)(13)(14)(15)(16)(17)(18)(19)(20). 55This process is thought to play a key role under oligotrophic conditions, where the 56 majority of microbes exist in a non-replicative, persistent state (14, 21). As the energy 57 requirements for persistence are approximately 1000-fold lower than for growing cells 58 (22), the energy provided by atmospheric H2 can theoretically sustain up to 10 8 cells 59 per gram of soil (23). 60The genetic basi...

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Section: Resultsmentioning

confidence: 99%

Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence

Cordero

Grinter

Hards

et al. 2019

Preprint

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“…Dihydrogen, as the most fundamental molecule, can serve as an energy source for microorganisms from a wide range of taxa and ecosystems (118,119). Soil microor-ganisms scavenge H 2 , which is present at atmospheric mixing ratios of 530 ppbv (120), as an electron donor for aerobic respiration (121).…”

Section: Continual-energy-harvesting Hypothesismentioning

confidence: 99%

Energetic Basis of Microbial Growth and Persistence in Desert Ecosystems

et al. 2020

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Microbial life is surprisingly abundant and diverse 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. Whereas photoautotrophs are restricted to specific niches in extreme deserts, metabolically versatile heterotrophs persist even in the hyper-arid topsoils of the Atacama Desert and Antarctica. At least three distinct strategies appear to allow such microorganisms to conserve energy in these oligotrophic environments: degradation of organic energy reserves, rhodopsin- and bacteriochlorophyll-dependent light harvesting, and oxidation of the atmospheric trace gases hydrogen and carbon monoxide. In turn, these principles are relevant for understanding the composition, functionality, and resilience of desert ecosystems, as well as predicting responses to the growing problem of desertification.

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“…Numerous studies have focused on the physiology of atmospheric H 2 scavenging during dormancy [10,11,14,27], but biochemical studies on the putative high-affinity Hyd-1h are scarce. Interestingly, the membrane association of the Hyd-1h seems to be essential for high-affinity atmospheric H 2 oxidation [12,14,15,27,31]. Indeed, the cytoplasmic Hyd-1h from R. eutropha H16 is a low-affinity enzyme, whereas whole cell studies in microbes with membrane-associated Hyd-1h show the contrary [12,18].…”

Section: Introductionmentioning

confidence: 99%

The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H2 with a high-affinity, membrane-associated [NiFe] hydrogenase

et al. 2020

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The trace amounts (0.53 ppmv) of atmospheric hydrogen gas (H 2 ) can be utilized by microorganisms to persist during dormancy. This process is catalyzed by certain Actinobacteria, Acidobacteria, and Chloroflexi, and is estimated to convert 75 × 10 12 g H 2 annually, which is half of the total atmospheric H 2 . This rapid atmospheric H 2 turnover is hypothesized to be catalyzed by high-affinity [NiFe] hydrogenases. However, apparent high-affinity H 2 oxidation has only been shown in whole cells, rather than for the purified enzyme. Here, we show that the membrane-associated hydrogenase from the thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV possesses a high apparent affinity (K m(app) = 140 nM) for H 2 and that methanotrophs can oxidize subatmospheric H 2 . Our findings add to the evidence that the group 1h [NiFe] hydrogenase is accountable for atmospheric H 2 oxidation and that it therefore could be a strong controlling factor in the global H 2 cycle. We show that the isolated enzyme possesses a lower affinity (K m = 300 nM) for H 2 than the membraneassociated enzyme. Hence, the membrane association seems essential for a high affinity for H 2 . The enzyme is extremely thermostable and remains folded up to 95°C. Strain SolV is the only known organism in which the group 1h [NiFe] hydrogenase is responsible for rapid growth on H 2 as sole energy source as well as oxidation of subatmospheric H 2 . The ability to conserve energy from H 2 could increase fitness of verrucomicrobial methanotrophs in geothermal ecosystems with varying CH 4 fluxes. We propose that H 2 oxidation can enhance growth of methanotrophs in aerated methane-driven ecosystems. Group 1h [NiFe] hydrogenases could therefore contribute to mitigation of global warming, since CH 4 is an important and extremely potent greenhouse gas.

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Molecular Hydrogen, a Neglected Key Driver of Soil Biogeochemical Processes

Cited by 55 publications

References 203 publications

Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence

Two uptake hydrogenases differentially interact with the aerobic respiratory chain during mycobacterial growth and persistence

Energetic Basis of Microbial Growth and Persistence in Desert Ecosystems

The thermoacidophilic methanotroph Methylacidiphilum fumariolicum SolV oxidizes subatmospheric H2 with a high-affinity, membrane-associated [NiFe] hydrogenase

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