Aquatic and terrestrial cyanobacteria produce methane

Abstract

Evidence is accumulating to challenge the paradigm that biogenic methanogenesis, considered a strictly anaerobic process, is exclusive to archaea. We demonstrate that cyanobacteria living in marine, freshwater, and terrestrial environments produce methane at substantial rates under light, dark, oxic, and anoxic conditions, linking methane production with light-driven primary productivity in a globally relevant and ancient group of photoautotrophs. Methane production, attributed to cyanobacteria using stable isotope labeling techniques, was enhanced during oxygenic photosynthesis. We suggest that the formation of methane by cyanobacteria contributes to methane accumulation in oxygen-saturated marine and limnic surface waters. In these environments, frequent cyanobacterial blooms are predicted to further increase because of global warming potentially having a direct positive feedback on climate change. We conclude that this newly identified source contributes to the current natural methane budget and most likely has been producing methane since cyanobacteria first evolved on Earth.

Fig. 1. δ¹³C-CH₄ values measured during incubation experiments of 13 different filamentous and unicellular freshwater, soil, and marine cyanobacterial cultures with and without NaH¹³CO₃ supplementation.

All cyanobacterial cultures produced CH₄. Using NaH¹³CO₃ as carbon source (CL) resulted in increasing stable δ¹³C-CH₄ values as compared to the starting condition. This establishes the direct link between carbon fixation and CH₄ production. The ¹³C enrichment is not quantitative and thus not comparable between cultures. Error bars represent SD (n = 4).

Fig. 2. Continuous measurements of CH₄ and oxygen under light/dark periods using a MIMS.

Examples are shown for two cultures. Data for other cultures can be found in fig. S2. A decrease in CH₄ concentration is a result of either reduced or no production coupled with degassing from the supersaturated, continuously mixing, semiopen incubation chamber toward equilibrium with atmospheric CH₄ (2.5 and 2.1 nM for fresh water and seawater, respectively). Calculated CH₄ production rates account for the continuous emission of CH₄ from the incubation chamber for as long as the CH₄ concentrations are supersaturated. The light regime for the experiments was as follows: Dark (black bars) from 19:30 to 09:00, and then light intensity (yellow bars) was programmed to increase to 60, 120, 180, 400 μmol quanta m⁻² s⁻¹ with a hold time of 1.5 hours at each light intensity. After the maximum light period, the light intensity was programmed to decrease in reversed order with the same hold times until complete darkness again at 19:30.

Fig. 3. Average CH₄ production rates obtained from multiple long-term measurements (2 to 5 days) using a MIMS.

The rates are designated by color according to the environment from which the cyanobacteria were originally isolated. Dark blue, marine environment; light blue, freshwater environment; green, soil environment. Gray and red lines represent median and mean values, respectively. Rates for the larger cyanobacteria in (A) are given in μmol g dry weight⁻¹ hour⁻¹ and rates for the picocyanobacteria (B) are given in pmol per 10⁶ cells per hour⁻¹.