Mixotrophy drives niche expansion of verrucomicrobial methanotrophs

Carere, Carlo R.; Hards, Kiel; Houghton, Karen M.; Power, Jean F.; McDonald, Ben; Collet, Christophe; Gapes, Daniel J.; Sparling, Richard; Boyd, Eric S.; Cook, Gregory M.; Greening, Chris; Stott, Matthew B.

doi:10.1038/ismej.2017.112

Cited by 101 publications

(123 citation statements)

References 63 publications

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“…However, cultivars most closely related to a Sulfurihydrogenibium species and to a Thermodesulfobacterium species were enriched for in the cultivation assays with

{NO}_{3}^{-}

for RSW3 and in the cultivation assay with

{SO}_{4}^{2 -}

for RSW1, respectively, and these could also potentially contribute to H 2 oxidation at these sites (Supporting information Table S8). Additionally, a recent study indicates that thermophilic methanotrophs can oxidize H 2 (Carere et al., ). However, 16S rRNA sequences affiliated with putative methanotrophs were not detected at significant abundances in any community in situ at RSE or RSW (>0.01% of the total community at each site, Figure ), suggesting these organisms are unlikely to represent a major hydrogen sink for H 2 .…”

Section: Discussionmentioning

confidence: 99%

Subsurface processes influence oxidant availability and chemoautotrophic hydrogen metabolism in Yellowstone hot springs

et al. 2018

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The geochemistry of hot springs and the availability of oxidants capable of supporting microbial metabolisms are influenced by subsurface processes including the separation of hydrothermal fluids into vapor and liquid phases. Here, we characterized the influence of geochemical variation and oxidant availability on the abundance, composition, and activity of hydrogen (H )-dependent chemoautotrophs along the outflow channels of two-paired hot springs in Yellowstone National Park. The hydrothermal fluid at Roadside East (RSE; 82.4°C, pH 3.0) is acidic due to vapor-phase input while the fluid at Roadside West (RSW; 68.1°C, pH 7.0) is circumneutral due to liquid-phase input. Most chemotrophic communities exhibited net rates of H oxidation, consistent with H support of primary productivity, with one chemotrophic community exhibiting a net rate of H production. Abundant H -oxidizing chemoautotrophs were supported by reduction in oxygen, elemental sulfur, sulfate, and nitrate in RSW and oxygen and ferric iron in RSE; O utilizing hydrogenotrophs increased in abundance down both outflow channels. Sequencing of 16S rRNA transcripts or genes from native sediments and dilution series incubations, respectively, suggests that members of the archaeal orders Sulfolobales, Desulfurococcales, and Thermoproteales are likely responsible for H oxidation in RSE, whereas members of the bacterial order Thermoflexales and the archaeal order Thermoproteales are likely responsible for H oxidation in RSW. These observations suggest that subsurface processes strongly influence spring chemistry and oxidant availability, which in turn select for unique assemblages of H oxidizing microorganisms. Therefore, these data point to the role of oxidant availability in shaping the ecology and evolution of hydrogenotrophic organisms.

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“…However, cultivars most closely related to a Sulfurihydrogenibium species and to a Thermodesulfobacterium species were enriched for in the cultivation assays with

{NO}_{3}^{-}

for RSW3 and in the cultivation assay with

{SO}_{4}^{2 -}

Section: Discussionmentioning

confidence: 99%

Subsurface processes influence oxidant availability and chemoautotrophic hydrogen metabolism in Yellowstone hot springs

et al. 2018

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“…Rates of H 2 oxidation or O 2 consumption were measured amperometrically according to previously established protocols (27, 30). For each set of measurements, either a Unisense H 2 microsensor or Unisense O 2 microsensor electrode were polarised at +800 mV or −800 mV, respectively, with a Unisense multimeter.…”

Section: Methodsmentioning

confidence: 99%

“…Representatives of three dominant soil phyla, Actinobacteriota, Acidobacteriota, and Chloroflexota, have been experimentally shown to oxidize atmospheric H 2 (3–5, 8, 24, 28, 29). Moreover, genomic and metagenomic studies indicate that at least 13 other phyla possess hydrogenases from lineages known to support atmospheric H 2 oxidation (13, 14, 19, 30).…”

Section: Introductionmentioning

confidence: 99%

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

Cordero

Grinter

Hards

et al. 2019

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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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“…For T. roseum cultures, rates of H 2 oxidation with and without treatment of respiratory chain uncouplers were measured amperometrically, following previously established protocols [49, 50]. Prior to the start of measurement, a Unisense H 2 microsensor electrode was polarised at +800 mV for 1 hr using a Unisense multimeter and calibrated with standards of known H 2 concentration.…”

Section: Methodsmentioning

confidence: 99%

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

Islam

Cordero

Feng

et al. 2018

Preprint

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23Bacteria within aerated environments often exist within a variety of dormant forms. In 24 these states, bacteria endure adverse environmental conditions such as organic 25 carbon starvation by decreasing metabolic expenditure and using alternative energy 26 sources. In this study, we investigated the energy sources that facilitate the 27 persistence of the environmentally widespread but understudied bacterial phylum 28 Chloroflexi. A transcriptome study revealed that Thermomicrobium roseum (class 29 Chloroflexia) extensively remodels its respiratory chain upon entry into stationary 30 phase due to organic carbon limitation. Whereas primary dehydrogenases associated 31 with heterotrophic respiration were downregulated, putative operons encoding 32 enzymes involved in molecular hydrogen (H2), carbon monoxide (CO), and sulfur 33 compound oxidation were significantly upregulated. Gas chromatography and 34 microsensor experiments were used to show that T. roseum aerobically respires H2 35 and CO at a range of environmentally relevant concentrations to sub-atmospheric 36 levels. Phylogenetic analysis suggests that the enzymes mediating atmospheric H2 37 and CO oxidation, namely group 1h [NiFe]-hydrogenases and type I carbon monoxide 38 dehydrogenases, are widely distributed in Chloroflexi genomes and have been 39 acquired on at least two occasions through separate horizontal gene transfer events. 40Consistently, we confirmed that the sporulating isolate Thermogemmatispora sp. T81 41(class Ktedonobacteria) also oxidises atmospheric H2 and CO during persistence. This 42 study provides the first axenic culture evidence that atmospheric CO supports bacterial 43 persistence and reports the third phylum to be experimentally shown to mediate the 44 biogeochemically and ecologically important process of atmospheric H2 oxidation. This 45 adds to the growing body of evidence that atmospheric trace gases serve as 46 dependable energy sources for the survival of dormant microorganisms. 47 48 49 Bacteria from the phylum Chloroflexi are widespread and abundant in free-living 50 microbial communities [1-4]. One reason for their success is their metabolic diversity; 51 cultured strains from the phylum include heterotrophs, lithotrophs, and phototrophs 52 adapted to both oxic and anoxic environments [5]. Cultured representatives of the 53 phylum are classified into four classes by the genome taxonomy database [6], the 54 primarily aerobic Chloroflexia and Ktedonobacteria and the anaerobic Anaerolineae 55 and Dehalococcoidia [5]. Numerous studies have provided insight into the metabolic 56 strategies anaerobic classes within Chloroflexi use to adapt to oligotrophic niches [7, 57 8]. Surprisingly little, however, is known about how aerobic heterotrophic bacteria 58 within this phylum colonise oxic environments. Global surveys have reported that 59 Chloroflexi comprise 4.3% of soil bacteria [2] and 3.2% of marine bacteria [3]. However, 60 the most dominant lineages within these ecosystems (notably Ellin6524 and SAR202) 61 have proven...

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Mixotrophy drives niche expansion of verrucomicrobial methanotrophs

Cited by 101 publications

References 63 publications

Subsurface processes influence oxidant availability and chemoautotrophic hydrogen metabolism in Yellowstone hot springs

Subsurface processes influence oxidant availability and chemoautotrophic hydrogen metabolism in Yellowstone hot springs

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

Two Chloroflexi classes independently evolved the ability to persist on atmospheric hydrogen and carbon monoxide

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