Proteomic Analysis of Methanococcus voltae Grown in the Presence of Mineral and Nonmineral Sources of Iron and Sulfur

Steward, Katherine F.; Payne, Devon; Kincannon, William M.; Johnson, Christina; Lensing, Malachi; Fausset, Hunter; Németh, Brigitta; Shepard, Eric M.; Broderick, William E.; Broderick, Joan B.; DuBois, Jennifer L.; Bothner, Brian

doi:10.1128/spectrum.01893-22

Cited by 4 publications

(2 citation statements)

References 82 publications

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“…This study provides the groundwork for the full elucidation of the mechanism utilized by Methanosarcina barkeri to access nutrients (Fe, S) from inert, Earth-abundant iron-sulfur minerals including FeS 2 . This work builds upon many previous analyses, including an analogous investigation on the proteome of Methanococcus voltae ( 27 ). Steward et al showed a greater degree of overall abundance changes (40% of identified proteins) in the comparison of M. voltae grown on FeS 2 compared with Fe(II)/HS − .…”

Section: Discussionmentioning

confidence: 90%

A shift between mineral and nonmineral sources of iron and sulfur causes proteome-wide changes in Methanosarcina barkeri

Fausset,

Spietz,

Cox

et al. 2024

Microbiol Spectr

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Iron (Fe) and sulfur (S) are required elements for life, and changes in their availability can limit the ecological distribution and function of microorganisms. In anoxic environments, soluble Fe typically exists as ferrous iron [Fe(II)] and S as sulfide (HS − ). These species exhibit a strong affinity that ultimately drives the formation of sedimentary pyrite (FeS 2 ). Recently, paradigm-shifting studies indicate that Fe and S in FeS 2 can be made bioavailable by methanogens through a reductive dissolution process. However, the impact of the utilization of FeS 2 , as opposed to canonical Fe and S sources, on the phenotype of cells is not fully understood. Here, shotgun proteomics was utilized to measure changes in the phenotype of Methanosarcina barkeri MS grown with FeS 2 , Fe(II)/HS − , or Fe(II)/cysteine. Shotgun proteomics tracked 1,019 proteins overall, with 307 observed to change between growth conditions. Functional characterization and pathway analyses revealed these changes to be systemic and largely tangential to Fe/S metabolism. As a final step, the proteomics data were viewed with respect to previously collected transcriptomics data to deepen the analysis. Presented here is evidence that M. barkeri adopts distinct phenotypes to exploit specific sources of Fe and S in its environment. This is supported by observed protein abundance changes across broad categories of cellular biology. DNA adjacent metabolism, central carbon metabolism methanogenesis, metal trafficking, quorum sensing, and porphyrin biosynthesis pathways are all features in the phenotypic differentiation. Differences in trace metal availability attributed to complexation with HS − , either as a component of the growth medium [Fe(II)/HS − ] or generated through reduction of FeS 2 , were likely a major factor underpinning these phenotypic differences. IMPORTANCE The methanogenic archaeon Methanosarcina barkeri holds great potential for industrial bio-mining and energy generation technologies. Much of the biochemistry of this microbe is poorly understood, and its characterization will provide a glimpse into biological processes that evolved close to life’s origin. The discovery of its ability to extract iron and sulfur from bulk, solid-phase minerals shifted a longstanding paradigm that these elements were inaccessible to biological systems. The full elucidation of this process has the potential to help scientists and engineers extract valuable metals from low-grade ore and mine waste generating energy in the form of methane while doing so.

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Section: Discussionmentioning

confidence: 90%

A shift between mineral and nonmineral sources of iron and sulfur causes proteome-wide changes in Methanosarcina barkeri

Fausset,

Spietz,

Cox

et al. 2024

Microbiol Spectr

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“…Deletion of Ehb hydrogenase changed the abundance of 10% of all detected proteins in comparison to the wild type ( 27 ). In M. voltae , iron and sulfur depletion affected the abundance of 40% of the proteome ( 33 ).…”

Section: Discussionmentioning

confidence: 99%

Proteomic and transcriptomic analysis of selenium utilization in Methanococcus maripaludis

Funkner,

Poehlein,

Jehmlich

et al. 2024

mSystems

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Methanococcus maripaludis utilizes selenocysteine- (Sec-) containing proteins (selenoproteins), mostly active in the organism’s primary energy metabolism, methanogenesis. During selenium depletion, M. maripaludis employs a set of enzymes containing cysteine (Cys) instead of Sec. The genes coding for these Sec-/Cys-containing isoforms were the only genes known of which expression is influenced by the selenium status of the cell. Using proteomics and transcriptomics, approx. 7% and 12%, respectively, of all genes/proteins were found differentially expressed/synthesized in response to the selenium supply. Some of the genes identified involve methanogenesis, nitrogenase functions, and putative transporters. An increase of transcript abundance for putative transporters under selenium depletion indicated the organism’s effort to tap into alternative sources of selenium. M. maripaludis is known to utilize selenite and dimethylselenide as selenium sources. To expand this list, a selenium-responsive reporter strain was assessed with nine other, environmentally relevant selenium species. While the effect of some was very similar to that of selenite, others were effectively utilized at lower concentrations. Conversely, selenate and seleno - amino acids were only utilized at unphysiologically high concentrations and two compounds were not utilized at all. To address the role of the selenium-regulated putative transporters, M. maripaludis mutant strains lacking one or two of the putative transporters were tested for the capability to utilize the different selenium species. Of the five putative transporters analyzed by loss-of-function mutagenesis, none appeared to be absolutely required for utilizing any of the selenium species tested, indicating they have redundant and/or overlapping specificities or are not dedicated selenium transporters. IMPORTANCE While selenium metabolism in microorganisms has been studied intensively in the past, global gene expression approaches have not been employed so far. Furthermore, the use of different selenium sources, widely environmentally interconvertible via biotic and abiotic processes, was also not extensively studied before. Methanococcus maripaludis JJ is ideally suited for such analyses, thanks to its known selenium usage and available genetic tools. Thus, an overall view on the selenium regulon of M. maripaludis was obtained via transcriptomic and proteomic analyses, which inspired further experimentation. This led to demonstrating the use of selenium sources M. maripaludis was previously not known to employ. Also, an attempt—although so far unsuccessful—was made to pinpoint potential selenium transporter genes, in order to deepen our understanding of trace element utilization in this important model organism.

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Biological conversion into bioethanol and biodiesel from municipal waste and future prospective w.r.t to circular economy

Garg,

Bala,

Tripathi

et al. 2024

Advances in Energy From Waste

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Proteomic Analysis of Methanococcus voltae Grown in the Presence of Mineral and Nonmineral Sources of Iron and Sulfur

Cited by 4 publications

References 82 publications

A shift between mineral and nonmineral sources of iron and sulfur causes proteome-wide changes in Methanosarcina barkeri

A shift between mineral and nonmineral sources of iron and sulfur causes proteome-wide changes in Methanosarcina barkeri

Proteomic and transcriptomic analysis of selenium utilization in Methanococcus maripaludis

Biological conversion into bioethanol and biodiesel from municipal waste and future prospective w.r.t to circular economy

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