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Novel niches for anaerobic methane oxidation and their biogeochemical sigificance

Periodic Reporting for period 4 - NOVAMOX (Novel niches for anaerobic methane oxidation and their biogeochemical sigificance)

Reporting period: 2021-04-01 to 2022-03-31

Motivated by a series of recent discoveries, NOVAMOX provides the first comprehensive biogeochemical and microbial ecological analysis of methane consumption in anoxic freshwater systems and oceanic oxygen minimum zones, environments where such processes to date were largely ignored. We hypothesize that anaerobic microbial methane oxidation pathways are important sinks in for methane in these environments, thereby affecting methane emissions and the cycling of nitrogen, iron, and sulfur, as the cycling of these elements is coupled either directly or indirectly to methane oxidation. With the development of new incubation and sensing techniques necessary to detect the processes in their environment, we will identify and quantify active pathways of anaerobic methane oxidation, identify the organisms that catalyse these transformations, analyse their environmental distribution, characterize kinetic controls of their growth and metabolic activity, and analyse the isotopic signatures they may leave behind. The project will generate robust estimates of the biogeochemical significance of anaerobic methane oxidation in these overlooked niches, and provide a quantitative mechanistic framework for analysis of the role of these processes in Earth’s biogeochemical evolution as well as for their implementation in forecasts of global change. The project will also provide fundamental new insights to the ecology of the highly specialized microorganisms involved in methane oxidation, for use in potential biotechnological applications.
During the project period, we have conducted intensive studies in both marine and freshwater systems. Investigations in marine systems included oceanic oxygen minimum zones (OMZs; oceanic waters where oxygen is depleted and anaerobic processes prevail) as well as coastal waters subject to permanent and seasonal oxygen depletion. We have studied methane cycling in the eastern tropical North Pacific and in the adjacent Golfo Dulce, Costa Rica, where waters with OMZ-like conditions are easily accessed. Our studies provide the first evidence for active methane consumption by anaerobic oxidation in the OMZ waters. The eastern tropical North Pacific holds the largest accumulation of methane in the open ocean, and our results imply that this methane pool is highly dynamic, and that consumption by anaerobic methane-oxidizing microbes is the main methane sink, substantially attenuating the transport of methane to surface water and eventually to the atmosphere.

In coastal waters subject to seasonal oxygen depletion, we similarly demonstrated how a highly efficient microbial community acts as a filter towards the release of the methane that accumulates in anoxic bottom waters. This is an important finding as these coastal “dead zones” are spreading and could represent a strong source of methane if such a filter did not exist.

This work required the development of highly sensitive methods to measure the microbial processes in the water column. While our measurements were conducted on samples recovered to the laboratory, we have also developed a system for incubation in situ, i.e. directly within the water column, in order to avoid potential artefacts resulting from sample recovery. The system will be of wide use in future studies of microbial processes in anoxic waters.

We have identified several different types of microbes that likely contribute to methane consumption in these systems. One surprising finding is that in oxygen-depleted coastal waters, methane oxidation is carried out by bacteria that are known as obligate aerobes, i.e. they are assumed to require oxygen for their metabolism. How these organisms manage to thrive in the absence of oxygen is a puzzle that remains to be solved. Our genomic investigations suggest that they may be able to use nitrogen compounds for their respiration as an alternative to oxygen. However, in a collaborative study, we also discovered that some microbes that are abundant in marine systems are able to produce oxygen under anoxic conditions. This may have very important implications for our understanding of the biogeochemistry of oxygen-depleted systems.

Freshwater systems make up a very important source of methane to the atmosphere, yet the mitigating impact of anaerobic methane oxidation on methane emissions was not known. We have determined rates of anaerobic methane oxidation at a range of different locations and explored how process rates depend on environmental parameters. We find that methane is oxidized anaerobically in diverse habitats and with an array of different oxidants including nitrate, nitrite, ferric iron, and sulfate. We also find that anaerobic methane oxidation in some settings efficiently traps methane and prevents its emission to the atmosphere. We have identified a group of microbes that appears to be of particular importance for oxidizing methane with iron and/or sulfate as electron acceptor, and we explored the ecophysiology of these organisms with both biogeochemical and molecular biological techniques. Based on this, we developed kinetic relationships that allows the inclusion of these processes in modellling of methane emissions from freshwater systems.
The project has provided new tools for investigation of methane cycling in diverse aquatic systems, as well as original new insights to the functioning of the methane cycle. Thus, our findings in oceanic oxygen minimum zones and coastal waters essentially launch methane cycling in anoxic marine waters as a new important field of research in marine biogeochemistry. The results not only demonstrate that methane is actively consumed, but also provide strong indications of a large and unknown source of methane in OMZs.

The identification and investigation of the microorganisms that consume methane in anoxic waters and the finding of oxygen production by microbes living in these systems opens a new field of research on cryptic oxygen cycling in anoxic systems with potentially wide-reaching implications for our understanding of element cycling in these systems.

Our results from freshwater systems demonstrate, for the first time, a wide distribution of anaerobic methane oxidation, which can be coupled to a diverse array of electron acceptors. The determination of the kinetics of these processes allows us to construct mathematical models to estimate the extent to which they attenuate methane fluxes, and how this function may vary in response to environmental change. These results can help to guide the environmental management of such systems towards a smaller greenhouse gas impact. Likewise, our identification of the organisms that carry out the processes, may potentially inspire biotechnological applications.
Water sampling in Golfo Dulce, Costa Rica in collaboration with colleagues from Universidad de Costa