Biotic interactions in microbial communities as modulators of biogeochemical processes : methanotrophy as a model system

Microbial interaction is an integral component of microbial ecology studies, yet the role, extent, and relevance of microbial interaction in community functioning remains unclear, particularly in the context of global biogeochemical cycles. While many studies have shed light on the physico-chemical cues affecting specific processes, (micro)biotic controls and interactions potentially steering microbial communities leading to altered functioning are less known. Yet, recent accumulating evidence suggests that the concerted actions of a community can be significantly different from the combined effects of individual microorganisms, giving rise to emergent properties. Here, we exemplify the importance of microbial interaction for ecosystem processes by analysis of a reasonably well-understood microbial guild, namely, aerobic methane-oxidizing bacteria (MOB). We reviewed the literature which provided compelling evidence for the relevance of microbial interaction in modulating methane oxidation. Support for microbial associations within methane-fed communities is sought by a re-analysis of literature data derived from stable isotope probing studies of various complex environmental settings. Putative positive interactions between active MOB and other microbes were assessed by a correlation network-based analysis with datasets covering diverse environments where closely interacting members of a consortium can potentially alter the methane oxidation activity. Although, methanotrophy is used as a model system, the fundamentals of our postulations may be applicable to other microbial guilds mediating other biogeochemical processes

Greenhouse gas (CO2, CH4, and N2O) emissions after abandonment of agriculture

The GHG (CO2, CH4, N2O) emission potential along a chronosequence of former agricultural soils abandoned for 9 to 32 years were compared to an actively managed (on-going) agricultural soil (reference). The soils were incubated in mesocosms with and without manure amendment, and microbial functional groups involved in nitrous oxide emission were quantitatively assessed. Carbon dioxide emission significantly increased after agriculture abandonment (< 24 years) consistent with higher decomposition rate, but total emission decreased in the long term (> 29 years). With the cessation of agriculture, the abandoned sites generally became a net methane sink. Notably, total nitrous oxide emission showed a significant monotonic decrease over years of abandonment in response to manure amendment, possibly reflecting an altered capacity for (de)nitrification as indicated in the response of the (de)nitrifier abundance. Overall, our findings suggest that the GHG legacy of agriculture diminishes over time (> 29 years), with lowered GHG emissions and global warming potential (GWP) after abandonment of agriculture. © 2022, The Author(s)

Pathways of methane removal in the sediment and water column of a seasonally anoxic eutrophic marine basin

Methane (CH4) is a key greenhouse gas. Coastal areas account for a major proportion of marine CH4 emissions. Eutrophication and associated bottom water hypoxia enhance CH4 production in coastal sediments. Here, we assess the fate of CH4 produced in sediments at a site in a seasonally anoxic eutrophic coastal marine basin (Scharendijke, Lake Grevelingen, the Netherlands) in spring (March) and late summer (September) in 2020. Removal of CH4 in the sediment through anaerobic oxidation with sulfate (Formula presented.) is known to be incomplete in this system, as confirmed here by only slightly higher values of δ13C-CH4 and δD-CH4 in the porewater in the shallow sulfate-methane-transition zone (~5-15 cm sediment depth) when compared to deeper sediment layers. In March 2020, when the water column was fully oxygenated, CH4 that escaped from the sediment was at least partially removed in the bottom water through aerobic oxidation. In September 2020, when the water column was anoxic below ~35 m water depth, CH4 accumulated to high concentrations (up to 73 µmol L-1) in the waters below the oxycline. The sharp counter gradient in oxygen and CH4 concentrations at ~35 m depth and increase in δ13C-CH4 and δD-CH4 above the oxycline indicate mostly aerobic water column removal of CH4. Water column profiles of particulate and dissolved Fe and Mn suggest redox cycling of both metals at the oxycline, pointing towards a potential role of metal oxides in CH4 removal. Water column profiles of (Formula presented.) and (Formula presented.) indicate removal of both solutes near the oxycline. Analyses of 16S rRNA gene sequences retrieved from the water column reveal the presence of aerobic CH4 oxidizing bacteria (Methylomonadaceae) and anaerobic methanotrophic archaea (Methanoperedenaceae), with the latter potentially capable of (Formula presented.) and/or metal-oxide dependent CH4 oxidation, near the oxycline. Overall, our results indicate sediment and water column removal of CH4 through a combination of aerobic and anaerobic pathways, which vary seasonally. Some of the CH4 appears to escape from the surface waters to the atmosphere, however. We conclude that eutrophication may make coastal waters a more important source of CH4 to the atmosphere than commonly assumed

Warming Can Boost Denitrification Disproportionately Due to Altered Oxygen Dynamics

Background: Global warming and the alteration of the global nitrogen cycle are major anthropogenic threats to the environment. Denitrification, the biological conversion of nitrate to gaseous nitrogen, removes a substantial fraction of the nitrogen from aquatic ecosystems, and can therefore help to reduce eutrophication effects. However, potential responses of denitrification to warming are poorly understood. Although several studies have reported increased denitrification rates with rising temperature, the impact of temperature on denitrification seems to vary widely between systems. Methodology/Principal Findings: We explored the effects of warming on denitrification rates using microcosm experiments, field measurements and a simple model approach. Our results suggest that a three degree temperature rise will double denitrification rates. By performing experiments at fixed oxygen concentrations as well as with oxygen concentrations varying freely with temperature, we demonstrate that this strong temperature dependence of denitrification can be explained by a systematic decrease of oxygen concentrations with rising temperature. Warming decreases oxygen concentrations due to reduced solubility, and more importantly, because respiration rates rise more steeply with temperature than photosynthesis. Conclusions/Significance: Our results show that denitrification rates in aquatic ecosystems are strongly temperature dependent, and that this is amplified by the temperature dependencies of photosynthesis and respiration. Our result

Resistance and Recovery of Methane-Oxidizing Communities Depends on Stress Regime and History; A Microcosm Study

Although soil microbes are responsible for important ecosystem functions, and soils are under increasing environmental pressure, little is known about their resistance and resilience to multiple stressors. Here, we test resistance and recovery of soil methaneoxidizing communities to two different, repeated, perturbations: soil drying, ammonium addition and their combination. In replicated soil microcosms we measured methane oxidation before and after perturbations, while monitoring microbial abundance and community composition using quantitative PCR assays for the bacterial 16S rRNA and pmoA gene, and sequencing of the bacterial 16S rRNA gene. Although microbial community composition changed after soil drying, methane oxidation rates recovered, even after four desiccation events. Moreover, microcosms subjected to soil drying recovered significantly better from ammonium addition compared to microcosms not subjected to soil drying. Our results show the flexibility of microbial communities, even if abundances of dominant populations drop, ecosystem functions can recover. In addition, a history of stress may induce changes in community composition and functioning, which may in turn affect its future tolerance to different stressors

Relief of phosphate limitation stimulates methane oxidation

Aquatic ecosystems such as shallow lakes and wetlands are important emitters of the greenhouse gas methane (CH4). Increased phosphorus (P) loading is expected to increase CH4 production in these ecosystems. This increased CH4 production can potentially be mitigated by increased CH4 oxidation, but how P availability affects methane-oxidizing bacterial (MOB) community composition and potential CH4 oxidation remains to be tested. Here, we incubated MOB from sediments of four subtropical lakes of different trophic states for 7 days at different phosphate (PO43-) concentrations to determine the effects of P on MOB community composition and potential CH4 oxidation. We measured CH4 consumption daily and compared CH4 oxidation during the exponential growth phase. Furthermore, we determined MOB community composition at the end of the incubations using qPCR of the pmoA gene. To test for differences in N and P uptake, we determined bacterial biomass N and P content. We found that increases in PO43- concentrations until 10 µM significantly increased CH4 oxidation. PO43- also increased bacterial biomass P content, while N content was not affected. MOB community composition was not affected by PO43- but more strongly correlated to lake of origin, likely due to the short duration of the incubations. Our results show that PO43- can not only stimulate CH4 oxidation indirectly through increased CH4 production, but also directly by increasing MOB growth. Importantly, these effects only occur at low PO43- concentrations, indicating that at high nutrient loads the increased CH4 oxidation will likely not mitigate the increased CH4 production