Methane production by three widespread marine phytoplankton species: release rates, precursor compounds, and potential relevance for the environment

Methane (CH4) production within the oceanic mixed layer is a widespread phenomenon, but the underlying mechanisms are still under debate. Marine algae might contribute to the observed CH4 oversaturation in oxic waters, but so far direct evidence for CH4 production by marine algae has only been provided for the coccolithophore Emiliania huxleyi. In the present study we investigated, next to E. huxleyi, other widespread haptophytes, i.e., Phaeocystis globosa and Chrysochromulina sp. We performed CH4 production and stable carbon isotope measurements and provide unambiguous evidence that all three investigated marine algae are involved in the production of CH4 under oxic conditions. Rates ranged from 1.9 ± 0.6 to 3.1 ± 0.4 µg of CH4 per gram of POC (particulate organic carbon) per day, with Chrysochromulina sp. and E. huxleyi showing the lowest and highest rates, respectively. Cellular CH4 production rates ranged from 16.8±6.5 (P. globosa) to 62.3±6.4 ag CH4 cell−1 d −1 (E. huxleyi; ag = 10−18 g). In cultures that were treated with 13C-labeled hydrogen carbonate, δ 13CH4 values increased with incubation time, resulting from the conversion of 13C– hydrogen carbonate to 13CH4. The addition of 13C-labeled dimethyl sulfide, dimethyl sulfoxide, and methionine sulfoxide – known algal metabolites that are ubiquitous in marine surface layers – resulted in the occurrence of 13C-enriched CH4 in cultures of E. huxleyi, clearly indicating that methylated sulfur compounds are also precursors of CH4. By comparing the algal CH4 production rates from our laboratory experiments with results previously reported in two field studies of the Pacific Ocean and the Baltic Sea, we might conclude that algae-mediated CH4 release is contributing to CH4 oversaturation in oxic waters. Therefore, we propose that haptophyte mediated CH4 production could be a common and important process in marine surface waters

Evidence for methane production by marine algae (Emiliana huxleyi) and its implication for the methane paradox in oxic waters

Methane (CH4), an important greenhouse gas that affects radiation balance and consequently the earth's climate, still has uncertainties in its sinks and sources. The world's oceans are considered to be a source of CH4 to the atmosphere, although the biogeochemical processes involved in its formation are not fully understood. Several recent studies provided strong evidence of CH4 production in oxic marine and freshwaters but its source is still a topic of debate. Studies of CH4 dynamics in surface waters of oceans and large lakes have concluded that pelagic CH4 supersaturation cannot be sustained either by lateral inputs from littoral or benthic inputs alone. However, frequently regional and temporal oversaturation of surface waters occurs. This comprises the observation of a CH4 oversaturating state within the surface mixed layer, sometimes also termed the "oceanic methane paradox". In this study we considered marine algae as a possible direct source of CH4. Therefore, the coccolithophore Emiliania huxleyi was grown under controlled laboratory conditions and supplemented with two 13C-labelled carbon substrates, namely bicarbonate and a position-specific 13C-labelled methionine (R-S-13CH3). The CH4 production was 0.7 μg POC g−1 d−1, or 30 ng g−1 POC h−1. After supplementation of the cultures with the 13C labelled substrate, the isotope label was observed in headspace-CH4. Moreover, the absence of methanogenic archaea within the algal culture and the oxic conditions during CH4 formation suggest that marine algae such as Emiliania huxleyi contribute to the observed spatial and temporal restricted CH4 oversaturation in ocean surface waters

Effects of Temperature and Light on Methane Production of Widespread Marine Phytoplankton

Methane (CH4) production in the ocean surface mixed layer is a widespread but still largely unexplained phenomenon. In this context marine algae have recently been described as a possible source of CH4 in surface waters. In the present study we investigated the effects of temperature and light intensity (including daylength) on CH4 formation from three widespread marine algal species Emiliania huxleyi, Phaeocystis globosa, and Chrysochromulina sp. Rates of E. huxleyi increased by 210% when temperature increased in a range from 10°C to 21.5°C, while a further increase in temperature (up to 23.8°C) showed reduction of CH4 production rates. Our results clearly showed that CH4 formation of E. huxleyi is controlled by light: When light intensity increased from 30 to 2,670 μmol m−2 s−1, CH4 emission rates increased continuously by almost 1 order of magnitude and was more than 1 order of magnitude higher when the daylength (light period) was extended from 6/18 hr light-dark cycle to continuous light. Furthermore, light intensity is also an important factor controlling CH4 emissions of Chrysochromulina sp. and P. globosa and could therefore be a species-independent regulator of phytoplankton CH4 production. Based on our results, we might conclude that extensive blooms of E. huxleyi could act as a main regional source of CH4 in surface water, since blooming of E. huxleyi is related to the seasonal increase in both light and temperature, which also stimulate CH4 production. Under typical global change scenarios, E. huxleyi will increase its CH4 production in the future

Methane formation driven by reactive oxygen species across all living organisms

Methane (CH4), the most abundant hydrocarbon in the atmosphere, originates largely from biogenic sources' linked to an increasing number of organisms occurring in oxic and anoxic environments. Traditionally, biogenic CH4 has been regarded as the final product of anoxic decomposition of organic matter by methanogenic archaea. However, plants(2,3), fungi(4), algae(5) and cyanobacteria(6) can produce CH4 in the presence of oxygen. Although methanogens are known to produce CH4 enzymatically during anaerobic energy metabolism(7), the requirements and pathways for CH4 production by non-methanogenic cells are poorly understood. Here, we demonstrate that CH4 formation by Bacillus subtilis and Escherichia coli is triggered by free iron and reactive oxygen species (ROS), which are generated by metabolic activity and enhanced by oxidative stress. ROS-induced methyl radicals, which are derived from organic compounds containing sulfur- or nitrogen-bonded methyl groups, are key intermediates that ultimately lead to CH4 production. We further show CH4 production by many other model organisms from the Bacteria, Archaea and Eukarya domains, including in several human cell lines. All these organisms respond to inducers of oxidative stress by enhanced CH4 formation. Our results imply that all living cells probably possess a common mechanism of CH4 formation that is based on interactions among ROS, iron and methyl donors, opening new perspectives for understanding biochemical CH4 formation and cycling

Aquatic and terrestrial cyanobacteria produce methane

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 EarthPeer reviewe

Stable Carbon Isotope Signature of Methane Released From Phytoplankton

AbstractAquatic ecosystems play an important role in global methane cycling and many field studies have reported methane supersaturation in the oxic surface mixed layer (SML) of the ocean and in the epilimnion of lakes. The origin of methane formed under oxic condition is hotly debated and several pathways have recently been offered to explain the “methane paradox.” In this context, stable isotope measurements have been applied to constrain methane sources in supersaturated oxygenated waters. Here we present stable carbon isotope signatures for six widespread marine phytoplankton species, three haptophyte algae and three cyanobacteria, incubated under laboratory conditions. The observed isotopic patterns implicate that methane formed by phytoplankton might be clearly distinguished from methane produced by methanogenic archaea. Comparing results from phytoplankton experiments with isotopic data from field measurements, suggests that algal and cyanobacterial populations may contribute substantially to methane formation observed in the SML of oceans and lakes.Plain Language Summary: Methane plays an important role in atmospheric chemistry and physics as it contributes to global warming and to the destruction of ozone in the stratosphere. Knowing the sources and sinks of methane in the environment is a prerequisite for understanding the global atmospheric methane cycle but also to better predict future climate change. Measurements of the stable carbon isotope composition of carbon—the ratio between the heavy and light stable isotope of carbon—help to identify methane sources in the environment and to distinguish them from other formation processes. We identified the carbon isotope fingerprint of methane released from phytoplankton including algal and cyanobacterial species. The observed isotope signature improves our understanding of methane cycling in the surface layers of aquatic environments helping us to better estimate methane emissions to the atmosphere.Key Points: Stable carbon isotope values of methane emitted from six phytoplankton cultures incubated in the laboratory. Isotope fractionation between methane source signature and biomass of widespread algal and cyanobacterial species. Isotopic patterns of methane released by phytoplankton may be clearly distinguished from methane formed by methanogenic archaea.Deutsche Forschungsgemeinschaft http://dx.doi.org/10.13039/501100001659Spanish Ministry of Universitieshttps://doi.org/10.11588/data/YYLEK

Stable Carbon Isotope Signature of Methane Released From Phytoplankton

Aquatic ecosystems play an important role in global methane cycling and many field studies have reported methane supersaturation in the oxic surface mixed layer (SML) of the ocean and in the epilimnion of lakes. The origin of methane formed under oxic condition is hotly debated and several pathways have recently been offered to explain the “methane paradox.” In this context, stable isotope measurements have been applied to constrain methane sources in supersaturated oxygenated waters. Here we present stable carbon isotope signatures for six widespread marine phytoplankton species, three haptophyte algae and three cyanobacteria, incubated under laboratory conditions. The observed isotopic patterns implicate that methane formed by phytoplankton might be clearly distinguished from methane produced by methanogenic archaea. Comparing results from phytoplankton experiments with isotopic data from field measurements, suggests that algal and cyanobacterial populations may contribute substantially to methane formation observed in the SML of oceans and lakes