A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

North, Justin A.; Narrowe, Adrienne B.; Xiong, Weili; Byerly, Kathryn M.; Zhao, Guanqi; Young, Sarah J.; Murali, Srividya; Wildenthal, John A.; Cannon, W. Roger; Wrighton, Kelly; Hettich, Robert L.; Tabita, F. Robert

doi:10.1126/science.abb6310

Cited by 60 publications

(57 citation statements)

References 63 publications

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“…This finding is interesting owing to recent indications that endophytic diazotrophs are essential for coniferous trees growing on nutrient‐poor soil (Moyes et al ., 2016; Puri et al ., 2020) and also considering cryptogamic covers, where cyanobacteria utilize these enzymes (Bellenger et al ., 2020). Furthermore, another nitrogenase‐type enzyme system, found in various microbial groups, was recently reported to produce CH 4 from dimethyl sulfide (North et al ., 2020), produced, for example, by various bacteria in terrestrial environments (Carrión et al ., 2015, 2017). Although the link between all of these nonarchaeal groups and CH 4 production in the living trees is uncertain, the aforementioned findings suggest that CH 4 formation in terrestrial ecosystems is a far more widespread trait than previously thought and also warrants their evaluation in the tree CH 4 studies.…”

Section: Current Understanding Of the Methane Production In Treesmentioning

confidence: 99%

New insight to the role of microbes in the methane exchange in trees: evidence from metagenomic sequencing

Putkinen

Siljanen

Laihonen³

et al. 2021

New Phytologist

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Methane (CH 4 ) exchange in tree stems and canopies and the processes involved are among the least understood components of the global CH 4 cycle. Recent studies have focused on quantifying tree stems as sources of CH 4 and understanding abiotic CH 4 emissions in plant canopies, with the role of microbial in situ CH 4 formation receiving less attention. Moreover, despite initial reports revealing CH 4 consumption, studies have not adequately evaluated the potential of microbial CH 4 oxidation within trees. In this paper, we discuss the current level of understanding on these processes. Further, we demonstrate the potential of novel metagenomic tools in revealing the involvement of microbes in the CH 4 exchange of plants, and particularly in boreal trees. We detected CH 4 -producing methanogens and novel monooxygenases, potentially involved in CH 4 consumption, in coniferous plants. In addition, our field flux measurements from Norway spruce (Picea abies) canopies demonstrate both net CH 4 emissions and uptake, giving further evidence that both production and consumption are relevant to the net CH 4 exchange. Our findings, together with the emerging diversity of novel CH 4 -producing microbial groups, strongly suggest microbial analyses should be integrated in the studies aiming to reveal the processes and drivers behind plant CH 4 exchange.

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Section: Current Understanding Of the Methane Production In Treesmentioning

confidence: 99%

New insight to the role of microbes in the methane exchange in trees: evidence from metagenomic sequencing

Putkinen

Siljanen

Laihonen³

et al. 2021

New Phytologist

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“…This is possibly occurring through the sulfhydrylation pathway, although details require further study. A third methionine synthesis pathway was recently discovered in freshwater and soil bacteria, although it is unlikely that this nitrogenase‐like enzyme is relevant here, as it is used only in sulfate‐limiting conditions 60 …”

Section: Resultsmentioning

confidence: 99%

Sulfur isotope analysis of cysteine and methionine via preparatory liquid chromatography and elemental analyzer isotope ratio mass spectrometry

Phillips

Sessions

2021

Rapid Comm Mass Spectrometry

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Sulfur isotope analysis of organic sulfur-containing molecules has previously been hindered by challenging preparatory chemistry and analytical requirements for large sample sizes. The natural-abundance sulfur isotopic compositions of the sulfur-containing amino acids, cysteine and methionine, have therefore not yet been investigated despite potential utility in biomedicine, ecology, oceanography, biogeochemistry, and other fields. Methods: Cysteine and methionine were subjected to hot acid hydrolysis followed by quantitative oxidation in performic acid to yield cysteic acid and methionine sulfone. These stable, oxidized products were then separated by reversed-phase high-performance liquid chromatography (HPLC) and verified via offline liquid chromatography/mass spectrometry (LC/MS). The sulfur isotope ratios (δ 34 S values) of purified analytes were then measured via combustion elemental analyzer coupled to isotope ratio mass spectrometry (EA/IRMS). The EA was equipped with a temperature-ramped chromatographic column and programmable helium carrier flow rates. Results: On-column focusing of SO 2 in the EA/IRMS system, combined with reduced He carrier flow during elution, greatly improved sensitivity, allowing precise (0.1-0.3‰ 1 s.d.) δ 34 S measurements of 1 to 10 μg sulfur. We validated that our method for purification of cysteine and methionine was negligibly fractionating using amino acid and protein standards. Proof-of-concept measurements of fish muscle tissue and bacteria demonstrated differences up to 4‰ between the δ 34 S values of cysteine and methionine that can be connected to biosynthetic pathways. Conclusions: We have developed a sensitive, precise method for measuring the natural-abundance sulfur isotopic compositions of cysteine and methionine isolated from biological samples. This capability opens up diverse applications of sulfur isotopes in amino acids and proteins, from use as a tracer in organisms and the environment, to fundamental aspects of metabolism and biosynthesis. 1 | INTRODUCTION The sulfur isotopic compositions of amino acids (AAs) are virtually unexplored but may hold significant utility across diverse scientific disciplines. In biomedicine, pilot studies have suggested that cysteine and methionine δ 34 S values could indicate disease progression as sulfur metabolism is dysregulated at the onset of liver cancer. 1 In archeology, bulk protein δ 34 S values of mummy hair 2 and mammalian collagen 3 have been used to reconstruct ancestral migration and reliance on fish protein, indicating this as a promising direction for

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“…Alternatively, CH 4 production may be catalyzed by DPOR and COR enzymes. Nitrogenases reduce a range of multi-bond compounds (59, 60, 61, 62, 63), and this quality is shared across different nitrogenases (64). We propose that, similar to the findings of Zheng et al (62), the nitrogenase-like enzymes DPOR and COR may be able to catalyze the reduction of CO2 into CH 4 when a suitable source of electrons is present.…”

Section: Resultsmentioning

confidence: 99%

Biogeochemical and omic evidence for paradoxical methane production via multiple co-occurring mechanisms in aquatic ecosystems

Perez‐Coronel

Beman

2020

Preprint

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Aquatic ecosystems are globally significant sources of the greenhouse gas methane (CH4) to the atmosphere. However, CH4 is produced ‘paradoxically’ in oxygenated water via at least three mechanisms, fundamentally limiting our understanding of overall CH4 production. Here we resolve these CH4 production mechanisms through CH4 measurements, δ13CH4 analyses, 16S rRNA sequencing, and metagenomics/transcriptomics applied to freshwater incubation experiments with multiple time points and treatments (addition of a methanogenesis inhibitor, dark, high-light). We captured significant paradoxical CH4 production, but show that methanogenesis was an unlikely CH4 source. In contrast, abundant freshwater bacteria metabolized methylphosphonate—similar to observations in marine ecosystems. Metatranscriptomics and stable isotopic analyses applied to experimental treatments also identified a potential CH4 production mechanism linked to (bacterio)chlorophyll metabolism by Cyanobacteria and especially Proteobacteria. Variability in these mechanisms across experiments indicates that multiple, widely-distributed bacterial groups and pathways can produce substantial quantities of CH4 in aquatic ecosystems.

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A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis

Cited by 60 publications

References 63 publications

New insight to the role of microbes in the methane exchange in trees: evidence from metagenomic sequencing

New insight to the role of microbes in the methane exchange in trees: evidence from metagenomic sequencing

Sulfur isotope analysis of cysteine and methionine via preparatory liquid chromatography and elemental analyzer isotope ratio mass spectrometry

Biogeochemical and omic evidence for paradoxical methane production via multiple co-occurring mechanisms in aquatic ecosystems

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