Impacts Of Peatland Microorganisms On Carbon Cycling Under Dry Conditions Revealed By Compound-specific Carbon Isotope Compositions Of Phospholipid Fatty Acids

Terrestrial ecosystems are important carbon sinks for atmospheric CO₂.Evaluating the carbon sequestration capacity and regulation mechanism of terrestrial ecosystems is important for achieving carbon neutrality.Among all terrestrial ecosystems,peatland has the largest carbon storage per unit area and the highest carbon density.Global peatlands cover only 3%of the land area but store about 600 billion tons of carbon.This carbon stock is equivalent to one-third of the total global soil organic carbon stock and70%of the current total atmospheric CO₂.Although peatlands are important carbon reservoirs,global peatlands are currently facing major threats from climate change and anthropogenic activities,such as peat mining,trenching and drainage,reclamation of farmland,and drought,which have led to a significant decline in the water level of peatlands.The water level decline changes the redox condition,impacting the activities of aerobic and anaerobic microorganisms,which further affect organic matter decomposition and greenhouse gas emissions in peatlands,and may change the carbon sink function of peatlands.Therefore,it is vital to understand how microbial activity changes with dry and water level decline,how it affects and regulates peatland carbon storage and greenhouse gas emissions,and what is the link between microbial activities and peatland carbon cycle processes.In the context of climate change and intensified anthropogenic activities,the above issues are of great significance to assess the carbon sink potential of peatlands and maintain the carbon sink function of peatlands.This thesis aims to understand the impact of microbial activity on peatland carbon cycling under dry and water level decline conditions at different time and spatial scales.Firstly,we carried out systematic monitoring of seasonal environmental parameters and carbon dynamics in Dajiuhu peatland in Shennongjia,Hubei Province,central China.By optimizing the purification and separation technology of microbial phospholipid fatty acids（PLFAs）and their compound-specific carbon isotope composition(δ¹³C)analysis,the response of microbial community structure and metabolic activity to seasonally dry conditions in Dajiuhu peatland were explored.At the same time,the impacts of microbial metabolic changes on particulate organic carbon content（POC）,dissolved organic carbon concentration（DOC）,and greenhouse gas emissions（CO₂and CH₄）were further studied.Secondly,we compared peatlands from different climatic zones with differences in wetness and dryness,including the British Tor Royal bog（50°N）in the north temperate zone,the Shennongjia Dajiuhu peatland（31°N）in the north subtropical zone,the subtropical Everglades peatland（26°N）in Florida,USA,and the Oropel peatland（9°N）in tropical Panama.We investigated spatial differences in microbial biomass,community structure,and carbon source utilization across the four peatlands,and the impact of these differences on POC,DOC,CO₂,and CH₄emissions.Finally,based on modern observations,we explored the impact of microbial activity on the peatland carbon cycle under dry climate conditions during geological history.By analyzing microbial lipids such as n-alkan-2-ones in peat deposits,I summarized the acidification process and microbial activity changes that may have occurred in 56peatlands around the world since the last deglaciation period,and explored the impact of microbial activity changes on carbon accumulation rates and atmospheric CH₄concentrations.The main conclusions drawn from these studies are as follows:（1）Under seasonal dry conditions,the microbial community structure and carbon metabolism activities changed rapidly in the Dajiuhu peatland.Gram-negative bacteria and actinomycetes increased during dry periods,while Gram-positive bacteria and fungi decreased.Changes in redox status caused by water level fluctuations may be responsible for microbial community structure changes.During dry and water level decline periods,theδ¹³C values??of microbial PLFAs were more negative by 1‰～5‰than in wet periods,with a maximum negative excursion of 12‰,indicating changes in microbial carbon utilization.Theδ¹³C values??of tentatively methanotrophic PLFAs,such as 18:1ω7c and 18:1ω9c,were most negative during dry periods,and theirδ¹³C values??were as low as–40‰,suggesting enhanced methanotrophy during dry periods.Except for methanotrophs,more negativeδ¹³C values??of non-methanotrophic PLFAs may be related to the secondary utilization of CH₄.According to the isotope mass balance calculation,more than 10%of the total microbial carbon source may come from CH₄during dry periods.Changes in microbial community structure and carbon utilization further significantly affected the carbon cycle process of the Dajiuhu peatland.Although the peat POC and CO₂emissions remained constant,the DOC concentration in the surface peat porewater decreased by an average of half during dry periods,accompanied by an increase in DOC humification.More importantly,the CH₄emission flux from the Dajiuhu peatland decreased significantly during dry periods and had negative values,indicating that the peatland was temporarily converted from a methane source to a methane sink.Besides the possible weakening of methanogenesis,enhanced methanotrophy during dry periods is likely to be a major reason for the dramatic reduction in CH₄emissions and the negative flux values,which is consistent with the more negativeδ¹³C value of methanotrophic PLFAs during dry periods.These observations suggest that under seasonal dry conditions,microorganisms can significantly affect carbon cycle processes in peatlands,and short-term moderate dry conditions may be beneficial for reducing CH₄emissions.（2）In the context of spatial differences,the total microbial biomass in the Tor Royal peatland in the north temperate zone was the lowest among the four peatlands.The microbial biomass in the Oropel peatland in the tropics was an order of magnitude higher than that in the Tor Royal peatland.The microbial community structure of the Tor Royal peatland was different from the other three peatlands,showing more Gram-negative bacteria and less Gram-positive bacteria than the others.The POC of the four peatlands showed a decreasing trend with increasing microbial biomass.Average DOC concentrations in the four peatlands showed a decreasing trend with lower water levels,consistent with seasonal dry-induced decreases in DOC concentrations.In terms of greenhouse gas emissions,the CO₂flux of the Dajiuhu peatland was the highest among the four peatlands,and the averageδ¹³C value of microbial PLFAs was also the most positive among the four peatlands.This suggests that the microbial heterotrophic consumption of organic matter in the Dajiuhu peatland may be responsible for the highest CO₂emissions.For CH₄emissions,the perennially flooded Everglades peatland had the highest CH₄fluxes,likely due to the high water level favoring methanogenesis activities.On the contrary,the CH₄flux of the Tor Royal peatland with water level 30cm below the surface was low.Theδ¹³C value of tentatively methanotrophic PLFAs in the Tor Royal peatland was as low as–38‰,indicating a possible active methanotrophy in the Tor Royal peatland.Moreover,theδ¹³C values of Sphagnum-derived fatty acids from the Tor Royal peatland were similar to those of methanotrophic PLFAs,suggesting that Sphagnum mosses may provide a symbiotic environment for methanotrophs.These results suggest that differences in microbial community structure and metabolic activities can result in different peatland carbon storage and greenhouse gas emissions at spatial scales.（3）During geological history,the paleohydrological proxies from previous studies indicate that the Dajiuhu peatland experienced dry events during the Early Holocene（11.6 ka～10.6 ka and 9.8 ka～9.4 ka）.The distribution of n-alkan-2-ones changed significantly during this period,indicating changes in microbial activities in the Dajiuhu peatland.The dry events during the Early Holocene also led to the acidification of the Dajiuhu peatland.Dry and acidification corresponded to the POC increase in the Dajiuhu peatland in the Early Holocene.Globally,56 peatlands from northern Europe,Alaska,eastern North America,northeastern and central-southern China,and South American Patagonia may also have experienced acidification and changes in microbial activity during the early to mid-Holocene.Peatland acidification in northern Europe,Alaska,and eastern North America may be associated with dry climates in the mid-to-high latitudes of the northern hemisphere during the Early Holocene.Dry and acidification may lead to changes in peatland methane cycling microorganisms,and methanotrophic activities may increase,leading to a decrease in global peatland CH₄emissions,which may be an important reason for the decline in atmospheric CH₄concentrations from the early to mid-Holocene.Acidification of peatlands also led to increased rates of carbon accumulation in these peatlands.These results suggest that peatland acidification and changes in microbial activity may have accelerated peatland carbon accumulation rates and reduced CH₄emissions in dry climates during geologically historical periods.The results of this thesis demonstrate that dry and water level decline can significantly affect the microbial community structure and carbon utilization in peatlands at seasonal,spatial,and geological historical scales,and these changes in microbial activity further significantly affect peatland solid（POC）,liquid（DOC）,gas（CO₂and CH₄）carbon cycle processes.According to the field observations and carbon budget balance calculations in this thesis,controlling the water level of peatlands at about 12～29 cm below the surface may be beneficial to significantly reduce CH₄emissions from peatlands without significantly increasing CO₂emissions.Through this water level management,it is estimated that the global peatlands can reduce equivalent CO₂emissions by about 450 to 520 million tons per year,thereby realizing the adding carbon sinks of peatlands.In the context of current climate change and intensified anthropogenic activities,global peatlands are expected to experience more frequent water level fluctuations and hydrological extremes,which may lead to rapid changes in microbial carbon metabolism activities,further altering the carbon sink function of peatlands.In the future,high-resolution monitoring of microbial activity in different types of peatlands is highly desirable.The microbiological mechanisms underlying the reduction of carbon emissions from peatlands on both seasonal and long-term scales need to be further explored to provide a better theoretical basis for“adding carbon sinks”and achieving“carbon neutrality”in terrestrial ecosystems.