4.6 Article

Oxygen Generation via Water Splitting by a Novel Biogenic Metal Ion-Binding Compound

Journal

APPLIED AND ENVIRONMENTAL MICROBIOLOGY
Volume 87, Issue 14, Pages -

Publisher

AMER SOC MICROBIOLOGY
DOI: 10.1128/AEM.00286-21

Keywords

methanobactin; chalkophore; water oxidation; methanotroph; aerobic methane oxidation; gold nanoparticle

Funding

  1. U.S. Department of Energy Office of Science [DE-SC0020174]
  2. National Science Foundation [1912482]
  3. Materials Science and Engineering Center at UW-Eau Claire
  4. ISU Bailey Research and Career Development
  5. U.S. Department of Energy (DOE) [DE-SC0020174] Funding Source: U.S. Department of Energy (DOE)
  6. Directorate For Engineering
  7. Div Of Chem, Bioeng, Env, & Transp Sys [1912482] Funding Source: National Science Foundation

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Methanobactins are small copper-binding peptides that can undergo reduction reactions with metal ions. Experimental evidence shows that the oxygen generated during metal ion reduction can support methane oxidation reactions.
Methanobactins (MBs) are small (<1,300-Da) posttranslationally modified copper-binding peptides and represent the extracellular component of a copper acquisition system in some methanotrophs. Interestingly, MBs can bind a range of metal ions, with some being reduced after binding, e.g., Cu-2(+) reduced to Cu+. Other metal ions, however, are bound but not reduced, e.g., K+. The source of electrons for selective metal ion reduction has been speculated to be water but never empirically shown. Here, using (H2O)-O-18, we show that when MBs from Methylocystis sp. strain SB2 (MB-SB2) and Methylosinus trichosporium OB3b (MB-OB3) were incubated in the presence of either Au3+, Cu-2, or Ag2+, O-1(8,)18(2) and free protons were released. No O-18,1(8)2 production was observed in the presence of either MB-SB2 or MB-OB3b alone, gold alone, copper alone, or silver alone or when K+ or Mo2+ was incubated with MB-SB2. In contrast to MB-OB3b, MB-SB2 binds Fe3+ with an N2S2 coordination and will also reduce Fe3+ to Fe-2(+). Iron reduction was also found to be coupled to the oxidation of 2H(2)O and the generation of O-2. MB-SB2 will also couple Hg-2(+), Ni2+, and Co2+ reduction to the oxidation of 2H(2)O and the generation of O-2, but MB-OB3b will not, ostensibly as MB-OB3b binds but does not reduce these metal ions. To determine if the O-2 generated during metal ion reduction by MB could be coupled to methane oxidation, (CH4)-C-13 oxidation by Methylosinus trichosporium OB3b was monitored under anoxic conditions. The results demonstrate that O-2 generation from metal ion reduction by MB-Mb can support methane oxidation. IMPORTANCE The discovery that MB will couple the oxidation of H2O to metal ion reduction and the release of O-2 suggests that methanotrophs expressing MB may be able to maintain their activity under hypoxidanoxic conditions through the self-generation of dioxygen required for the initial oxidation of methane to methanol. Such an ability may be an important factor in enabling methanotrophs to not only colonize the oxic-anoxic interface where methane concentrations are highest but also tolerate significant temporal fluctuations of this interface. Given that genomic surveys often show evidence of aerobic methanotrophs within anoxic zones, the ability to express MB (and thereby generate dioxygen) may be an important parameter in facilitating their ability to remove methane, a potent greenhouse gas, before it enters the atmosphere.

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