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Multiple sources of aerobic methane production in aquatic ecosystems include bacterial photosynthesis - PubMed

  • ️Sat Jan 01 2022

Multiple sources of aerobic methane production in aquatic ecosystems include bacterial photosynthesis

Elisabet Perez-Coronel et al. Nat Commun. 2022.

Abstract

Aquatic ecosystems are globally significant sources of the greenhouse gas methane to the atmosphere. Until recently, methane production was thought to be a strictly anaerobic process confined primarily to anoxic sediments. However, supersaturation of methane in oxygenated waters has been consistently observed in lakes and the ocean (termed the 'methane paradox'), indicating that methane can be produced under oxic conditions through unclear mechanisms. Here we show aerobic methane production from multiple sources in freshwater incubation experiments under different treatments and based on biogeochemical, metagenomic, and metatranscriptomic data. We find that aerobic methane production appears to be associated with (bacterio)chlorophyll metabolism and photosynthesis, as well as with Proteobacterial degradation of methylphosphonate. Genes encoding pathways for putative photosynthetic- and methylphosphonate-based methane production also co-occur in Proteobacterial metagenome-assembled genomes. Our findings provide insight into known mechanisms of aerobic methane production, and suggest a potential co-occurring mechanism associated with bacterial photosynthesis in aquatic ecosystems.

© 2022. The Author(s).

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1. Methane (CH4) production or consumption rates across experiments.

Different colors represent different treatments or control incubations. Different symbols denote the year of the experiment. Abbreviations at left denote lake (Lukens =L, Lower Cathedral =LC, Upper Cathedral =UC, Lower Gaylor =LG, and Upper Gaylor =UG) and experiment number in each lake (e.g., UC4 is the fourth experiment in Upper Cathedral Lake). Rates were calculated from the slopes of significant (P < 0.05) correlations between time and triplicate CH4 concentration measurements conducted at multiple timepoints during experimental incubations. Where symbols are not shown, asterisks indicate that no significant production or consumption occurred. Error bars denote standard errors of slope values for significant correlations between CH4 and time; in some cases, these are smaller than the datapoints and are not visible. BES indicates the addition of the methanogenesis inhibitor 2-bromoethanesulphonate. Source data are provided as a Source Data file.

Fig. 2
Fig. 2. Functional genes in metatranscriptomes and metagenomes.

Variations across experiments and treatments in (a) transcript abundance (normalized as % of DNA recombination protein (recA) transcripts in metatranscriptomes) and (b) gene abundance (normalized as % of recA genes in metagenomes) of key functional genes. Functional genes quantified include those involved in: methane oxidation (particulate methane monooxygenase; pmoA), methanogenesis (methyl coenzyme M reductase; mcrA), phosphonate assimilation (C-P lyase and phosphonate-binding protein; phnJ and phnD), and phosphonate synthesis (phosphoenolpyruvate mutase and phosphonopyruvate decarboxylase; pepM and ppd). Abbreviations denote the experiment (e.g., UC4), the treatment (control, addition of the methanogenesis inhibitor 2-bromoethanesulphonate [BES], or high light intensity), and the sampling time point (t0 indicates initial sampling time point and tf indicates endpoint sample). Note the difference in the vertical axis for the LG5 experiment in comparison with the other experiments. Source data are provided as a Source Data file.

Fig. 3
Fig. 3. δ13CH4 and CH4 in experimental treatments.

δ13CH4 values are shown over time for duplicate samples collected during the (a) L7, (b) LG6, and c UC4 and UC3 experiments. d CH4 concentrations are shown over time in the UC4 experiment. Different colors denote different experimental treatments and controls (BES indicates the addition of the methanogenesis inhibitor 2-bromoethanesulphonate). Scales of the vertical axes differ between experiments in a–c. In (c), the triangle denotes the UC3 BES treatment; controls are not shown due to a lack of change. In d, error bars denote the standard deviation of the mean of triplicate concentration measurements; in some cases, these are smaller than the datapoints and are not visible. Source data are provided as a Source Data file.

Fig. 4
Fig. 4. Gene expression in the UC4 experimental treatments compared with the control.

Functional genes involved in methanogenesis (methyl coenzyme M reductase; mcrA), phosphonate assimilation (phosphonate-binding protein and C-P lyase; phnD and phnJ), phosphonate synthesis (phosphoenolpyruvate mutase and phosphonopyruvate decarboxylase; pepM and ppd), and porphyrin and chlorophyll metabolism (ferredoxin:protochlorophyllide reductase and chlorophyllide reductase; DPOR and COR) are shown. The BES treatment (addition of the methanogenesis inhibitor 2-bromoethanesulphonate) is shown in the top panel and the high light treatment in the bottom panel. Each panel shows the net effect of the treatment on the different genes in metatranscriptomes. DNA recombination protein (recA) transcripts are also shown for comparison. Source data are provided as a Source Data file.

Fig. 5
Fig. 5. Expression and abundance of bacterial photosynthesis genes.

Protochlorophyllide reductase (DPOR) and chlorophyllide reductase (COR) reads in a metatranscriptomes, (b) metagenomes, and c mapped to the Limnohabitans metagenome-assembled genome (MAG) 5. In a, b, DPOR (red) and COR (blue) transcripts (a) and genes (b) are shown within different experiments and experimental treatments. Abbreviations denote the experiment (e.g., UC4), the sampling time point, and the treatment (control, addition of the methanogenesis inhibitor 2-bromoethanesulphonate [BES], or high light intensity). In c, the Limnohabitans MAG 5 is shown in circular form, and the number of reads mapping to genes within the MAG are indicated by color intensity. Different experiments and treatments are shown in different colors, with the LG6 experiment in red, L7 in orange, the UC4 control in aqua, the UC4 BES treatment in light blue, and the UC4 high light treatment in dark blue. Locations of DPOR and COR (and associated photosynthesis genes) within the MAG are indicated. Source data are provided as a Source Data file.

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