Microbial Methane From Methylphosphonate Isotopically Records Source

Abstract

Methane is a potent greenhouse gas commonly supersaturated in the oxic surfaces waters of oceans and lakes, yet canonical microbial methanogens are obligate anaerobes. One proposed methane production pathway involves microbial degradation of methylphosphonate (MPn), which can proceed in the presence of oxygen. Directly tracing dissolved methane to its source in oxic waters, however, remains a challenge. To address this knowledge gap, we quantified the carbon isotopic fractionation between substrate MPn and product methane (1.3‰) in lab experiments, which was 1 to 2 orders of magnitude smaller than canonical pathways of microbial methanogenesis (20 to 100‰). Together, these results indicated that microbial catabolism of MPn is a source of methane in surface oceans and lake waters, but to differentiate sources of MPn in nature a further accounting of all sources is necessary. Methane from this pathway must be considered in constraining the marine carbon cycle and methane budget.

Large Hydrogen Isotope Fractionation Distinguishes Nitrogenase-Derived Methane from Other Methane Sources

“…Over the past decade, it has been recognized that minor additional contributions of methane derive from the demethylation of organophosphonates (c.f. (6)(7)(8)) and from inefficient Wood-Ljungdahl pathway carbon fixation (9). Most recently, it was discovered that some forms of the metalloenzyme nitrogenase also reduce carbon dioxide (CO2) into methane (10).…”

“…Previous research has established that each form of nitrogenase imparts a characteristic nitrogen or carbon isotope fractionation during N2 (34) or acetylene (27) reduction, respectively. The stable isotopes of carbon ( 13 C/ 12 C) and hydrogen ( 2 H/ 1 H) are commonly used to differentiate ('fingerprint') different sources of methane (2,8,(35)(36)(37)(38)(39)(40). To determine what characteristic carbon and hydrogen isotope fractionations are associated with methane production by the different nitrogenases, we cultivated V-and Fe-only nitrogenase utilizing strains of the anoxygenic photoheterotroph Rhodopseudomonas palustris under nitrogen fixing conditions.…”

“…The primary function of Mcr is for catabolism, with methane production thought to occur only after other more favorable electron acceptors, like oxygen, nitrate, or sulfate, have been consumed ( 3 – 5 ). Over the past decade, it has been recognized that minor additional contributions of methane derive from the demethylation of organophosphonates ( 6 – 8 ) and from inefficient Wood-Ljungdahl pathway carbon fixation ( 9 ). Most recently, it was discovered that some forms of the metalloenzyme nitrogenase also reduce carbon dioxide (CO 2 ) into methane ( 10 ).…”

“…These findings beg the question of whether and to what extent carbon dioxide reduction by nitrogenase is an important methane source in certain environments and how to distinguish nitrogenase-derived methane from other sources. The stable isotopes of carbon ( 13 C/ 12 C) and hydrogen ( 2 H/ 1 H) are commonly used to differentiate (fingerprint) different sources of methane ( 2 , 8 , 35 – 40 ). Previous research has established that each form of nitrogenase imparts a characteristic nitrogen or carbon isotope fractionation during N 2 ( 34 ) or acetylene ( 27 ) reduction, respectively.…”

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

“…2) in these treatments suggest another source. Strong isotopic fractionation from MPn also seems unlikely, as the mean isotopic fractionation for CH4 derived from MPn by the cleavage of the C-P bond is only 1.3‰ (Taenzer et al 2020). MPn could be allochthonous (terrestrial) or autochthonous (based on pepM results), but in either case, is unlikely to be so 13 C-depleted.…”