Transcriptional regulation of methanogenic metabolism in archaea

Shalvarjian, Katie E; Nayak, Dipti D

doi:10.1016/j.mib.2021.01.005

Cited by 13 publications

(6 citation statements)

References 55 publications

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“…6b). Genes involved in methanogenesis are considered to be transcriptionally regulated in response to both extracellular and intracellular signals [44]. The regulation of Mta by the methanol-speci c-regulators (Msr) is one of the few regulators recognized so far [45].…”

Section: Discussionmentioning

confidence: 99%

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Huang,

Tang,

Zhao

et al. 2023

Microb Ecol

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Biochar is ubiquitous in diverse natural and engineered anaerobic systems. The biogeochemical roles of biochar during its production, storage and dynamics show an involvement in the global methane ux that is governed by methanotrophs and methanogens. Understanding of the relevant mechanisms is currently restricted to the roles of biochar in the methanotrophic growth but less is known of the roles in methanogenic growth. Here, we demonstrated that biochar enhanced methanogenic growth of a model methanogen Methanosarcina acetivorans, and the role of biochar as an electron acceptor during the methanogenic growth was con rmed, referring as biochar-respiratory growth. The biochar-respiratory growth of M. acetivorans promoted the secretion of extracellular polymeric substances (EPS) with augmented electron transfer capability, and the removal of EPS signi cantly attenuated extracellular electron transfer. Identi cation and quanti cation of prosthetic cofactors for EPS suggest an important role of avin and F 420 in the extracellular electron transfer. Transcriptomic analysis provided more insights into the biochar-respiratory growth of M. acetivorans to show that transcriptional regulation positively responded to the favorable growth environment provided by biochar, thereby stimulating global methanogenesis. Our results enlighten the in situ roles of biochar in the ecophysiology of methanogens in diverse anaerobic environments.

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Section: Discussionmentioning

confidence: 99%

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Huang,

Tang,

Zhao

et al. 2023

Microb Ecol

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“…Ca 2+ ions are well‐studied communicators that bind numerous messenger proteins to initiate stress‐signaling and metabolic responses (Carafoli & Krebs, 2016). The duration of stress‐signaling and processing ranges from a few seconds for initial signaling to an hour for complete metabolic transition; factors such as stressor type and dose, as well as exposure period, influence the cells' response timing (Barrán‐Berdón et al, 2011; Carafoli & Krebs, 2016; Hotamisligil & Davis, 2016; Shalvarjian & Nayak, 2021). We implemented the threshold effects in the model in two stages.…”

Section: Methodsmentioning

confidence: 99%

Microbiological hydrogen (H₂) thresholds in anaerobic continuous‐flow systems: Effects of system characteristics

Karadagli

Marcus

Rittmann

2023

Biotech & Bioengineering

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Hydrogen (H 2 ) concentrations that were associated with microbiological respiratory processes (RPs) such as sulfate reduction and methanogenesis were quantified in continuous-flow systems (CFSs) (e.g., bioreactors, sediments). Gibbs free energy yield (ΔG ́~0) of the relevant RP has been proposed to control the observed H 2 concentrations, but most of the reported values do not align with the proposed energetic trends. Alternatively, we postulate that system characteristics of each experimental design influence all system components including H 2 concentrations. To analyze this proposal, a Monod-based mathematical model was developed and used to design a gas-liquid bioreactor for hydrogenotrophic methanogenesis with Methanobacterium bryantii M.o.H. Gas-to-liquid H 2 mass transfer, microbiological H 2 consumption, biomass growth, methane formation, and Gibbs free energy yields were evaluated systematically. Combining model predictions and experimental results revealed that an initially large biomass concentration created transients during which biomass consumed [H 2 ] L rapidly to the thermodynamic H 2 -threshold (≤1 nM) that triggerred the microorganisms to stop H 2 oxidation. With no H 2 oxidation, continuous gas-to-liquid H 2 transfer increased [H 2 ] L to a level that signaled the methanogens to resume H 2 oxidation. Thus, an oscillatory H 2concentration profile developed between the thermodynamic H 2 -threshold (≤1 nM) and a low [H 2 ] L (~10 nM) that relied on the rate of gas-to-liquid H 2transfer. The transient [H 2 ] L values were too low to support biomass synthesis that could balance biomass losses through endogenous oxidation and advection; thus, biomass declined continuously and disappeared. A stable [H 2 ] L (1807 nM) emerged as a result of abiotic H 2 -balance between gas-to-liquid H 2 transfer and H 2 removal via advection of liquid-phase.

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“…As some Methanosarcina species can utilize different substrates to obtain the energy necessary to grow, it would be plausible that distinct regulatory mechanisms can either stimulate or inhibit the transcription of key enzymes of different methanogenic pathways when the substrate changes ( 11 , 12 ). For instance, in Methanosarcina acetivorans , MsrA, and MsrB can activate the mtaCB1 operon, whereas both MsrD and MsrE can activate the mtaCB2 operon and repress the mtaCB3 operon ( 13 ).…”

Section: Introductionmentioning

confidence: 99%

The novel regulator HdrR controls the transcription of the heterodisulfide reductase operon hdrBCA in Methanosarcina barkeri

Zhang,

Chen,

Wang

et al. 2024

Appl Environ Microbiol

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Methanogenic archaea play a key role in the global carbon cycle because these microorganisms remineralize organic compounds in various anaerobic environments. The microorganism Methanosarcina barkeri is a metabolically versatile methanogen, which can utilize acetate, methanol, and H 2 /CO 2 to synthesize methane. However, the regulatory mechanisms underlying methanogenesis for different substrates remain unknown. In this study, RNA-seq analysis was used to investigate M. barkeri growth and gene transcription under different substrate regimes. According to the results, M. barkeri showed the best growth under methanol, followed by H 2 /CO 2 and acetate, and these findings corresponded well with the observed variations in genes transcription abundance for different substrates. In addition, we identified a novel regulator, MSBRM_RS03855 (designated as HdrR), which specifically activates the transcription of the heterodisulfide reductase hdrBCA operon in M. barkeri . HdrR was able to bind to the hdrBCA operon promoter to regulate transcription. Furthermore, the structural model analyses revealed a helix-turn-helix domain, which is likely involved in DNA binding. Taken together, HdrR serves as a model to reveal how certain regulatory factors control the expression of key enzymes in the methanogenic pathway. IMPORTANCE The microorganism Methanosarcina barkeri has a pivotal role in the global carbon cycle and contributes to global temperature homeostasis. The consequences of biological methanogenesis are far-reaching, including impacts on atmospheric methane and CO 2 concentrations, agriculture, energy production, waste treatment, and human health. As such, reducing methane emissions is crucial to meeting set climate goals. The methanogenic activity of certain microorganisms can be drastically reduced by inhibiting the transcription of the hdrBCA operon, which encodes heterodisulfide reductases. Here, we provide novel insight into the mechanisms regulating hdrBCA operon transcription in the model methanogen M. barkeri . The results clarified that HdrR serves as a regulator of heterodisulfide reductase hdrBCA operon transcription during methanogenesis, which expands our understanding of the unique regulatory mechanisms that govern methanogenesis. The findings presented in this study can further our understanding of how genetic regulation can effectively reduce the methane emissions caused by methanogens.

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Transcriptional regulation of methanogenic metabolism in archaea

Cited by 13 publications

References 55 publications

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Microbiological hydrogen (H₂) thresholds in anaerobic continuous‐flow systems: Effects of system characteristics

The novel regulator HdrR controls the transcription of the heterodisulfide reductase operon hdrBCA in Methanosarcina barkeri

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Transcriptional regulation of methanogenic metabolism in archaea

Cited by 13 publications

References 55 publications

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Unveiling the Biochar-Respiratory Growth of Methanosarcina acetivorans Involving Extracellular Polymeric Substances

Microbiological hydrogen (H2) thresholds in anaerobic continuous‐flow systems: Effects of system characteristics

The novel regulator HdrR controls the transcription of the heterodisulfide reductase operon hdrBCA in Methanosarcina barkeri

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Microbiological hydrogen (H₂) thresholds in anaerobic continuous‐flow systems: Effects of system characteristics