Wetland Biogeochemistry Biology 643: Biogeochemistry Allison Gill Nov. 20, 23, 30 2015

Outline Introduction to wetlands II. Wetland C Cycling Primary Production Decomposition Aerobic Anaerobic III. Global change in high latitude wetlands IV: Case Study – SPRUCE Experiment

Wetland Terrestrial system with water at or near the soil surface for all or part of the year Tropical Peat Bog Temperate coastal salt marsh Wetlands are terrestrial systems in which water is at or near the soil surface for all or part of the year There are lots of different types of wetlands which occur all over the world Peat forests in the tropics, many of which have been degraded for palm oil plantations, mangrove swamps in subtropical coastal areas, salt marshes in coastal temperate zones, fens and bogs at high latitudes, among many others All of these are widely different ecosystems, but are united by the transient or continuous characteristic of water saturation, which defines the biogeochemical nature of wetland systems Water diffuses 10,000 times more slowly in water than air, therefore oxygen is far less abundant than in non-wetland ecosystems Typically oxygen is consumed faster than it can diffuse through water columns and water-saturated substrates, so systems are typically anoxic and plants and microbes that live there developed to metabolize under those conditions Subtropical Mangrove Swamp Boreal Fen

Wetland Distribution 5-12 x 10-6 km2 7-15% land area hard to accurately assess the spatial extent of wetlands In general, binned into different types based on features of hydrology, vegetation, and soils but global estimatesa re that they are about 5 to 12 million square kilometers, most are in cold high latitude ecosystems are a relatively small proportion of the land area, but store the majority of global soil C are also a major methane source, comprise about 20-30% of methane emissions 5-12 x 10-6 km2 7-15% land area >50% global soil C 20-33% global CH4 emissions

Nature Climate Change Oct 2013 because wetlands play a disproportionate role in the carbon cycle in terms of the size of the belowground pool and the methane flux, are of major interest in to climate change in particular, a lot of interest to understand the unique biogeochemistry of these systems so we can think about how the giant carbon store might be affected by CC. Will it remain stored as organic material, exported as DOC, or released as gaseous C? Will that gaseous C be CO2 or methane? How fast will it come out? Nature Climate Change Oct 2013

Wetland characteristics are primarily defined by hydrology and water source Water Enters: Precipitation Groundwater Surface Flow/Run-off Water Leaves: Evapotranspiration Groundwater recharge Surface outflow Residence Time is the average amount of time a unit of water remains in the wetland So lets talk a little bit about the hydrology of wetland systems, as that is a major factor that defines the current state of wetlands and will influence future C storage Beyond just the presence of water, the source of the water influences the biogeochemical nature of each system Both the source of the water and the time a particular molecule of water remains in the wetland can vary greatly Water enters and leaves through a variety of mechanisms

Wetland characteristics are primarily defined by hydrology and water source Brinson et al. 1993 7

Wetland characteristics are primarily defined by hydrology and water source Precip-dominated wetlands Long residence times “Closed systems” Biogeochemically isolated from catchment Wetlands that get most of the water from precipitation tend to have water that has a very long residence time in the system, thought of as “closed”, are biogeochemically isolated from the catchment. Systems tend to be quite nutrient poor, have slow-growing plant species adapted to oligotrophic conditions Brinson et al. 1993 8

Bog

Wetland characteristics are primarily defined by hydrology and water source Groundwater wetlands Shorter residence times Nutrient input from/DOC export to catchment wetlands with a strong groundwater source tend to have shorter water residence times. The groundwater brings nutrients into the wetland from the surrounding watershed and the wetland tends to export DOC. Because of the nutrient source, these wetlands tend to support different plant communities Brinson et al. 1993 10

Fen

Wetland characteristics are primarily defined by hydrology and water source Surface Flow Wetlands Shorter residence times Sediment & nutrient input Sometimes saline, reduces O2 solubility and species diversity wetlands that are influenced by surface flow also have short residence times, although it can be variable if it is something like a seasonally-flooded system or a tidal ecosystem often get sediment and nutrient input from surrounding hydrological system many tidal systems are saline, tends to reduce O2 solubility and plant species diversity since relatively few plants can deal with fluctuating osmolarity Brinson et al. 1993 12

Tidal Marsh www.maine.gov

Primary Productivity in Wetlands Water saturation and anoxia creates unique metabolic environment for present plant and microbial community Higher plants need oxygen for root growth Morphological adaptations to access O2 plant growth in wetlands is source of soil C in wetlands water saturation and anoxia creates unique metabolic environment for present plant and microbial community higher plants need oxygen for root growth Some plants have developed physiological adaptations to deal with oxygen limitation – sedges have aerenchymous tissue that allow oxygen to diffuse below the water surface and mangrove species have pneumatophores, or root structures that reach above the surface to access oxygen. In oligotrophic systems, such as bogs, non-vascular Sphagnum spp outcompete vascular plants. Sphagnum do not have true roots and take up water and nutrients though diffusion into hyaline cells, which allows them to proliferate in strongly water-rich and nutrient limited environments. Once present, Sphagnum has extremely recalcitrant litter that decomposes slowly, and also has high hydraulic conductivity, feeding back on water saturation, anoxia, and organic matter accumulation in the wetland. Sedge aerenchyma Mangrove pneumatophores Nonvascular Sphagnum

Wetlands and the C Cycle Photosynthesis and Primary Production will step through unique aspects of wetland carbon cycling that influence the nature of carbon storage and fluxes I am going to use this summary figure which does a nice job highlighting all the interacting fluxes We’ll start with photosynthesis. Plants take up CO2 which they use to generate the complex organic compounds that are a part of plant tissue. O2 is generated as a byproduct

Wetlands and the C Cycle Decomposition impeded in anoxic soils Many wetlands have accumulated large SOM stocks Major global carbon store Plant material still recognizable -> PEAT Acrotelm: aerobic portion of peat profile above the water table. Aerated with roots, recent plant litter inputs, less decomposed, most microbial activity, higher hydraulic conductivity Catotelm: portion of the profile below the water surface Proportion of peat entering the catotelm depends on burial rate and residence time of litter you guys talked about the carbon cycle already, and are aware that as plants die, the complex organic material is broken down and used as energy by soil microbes this is fundamentally the case in wetlands, but the processes are somewhat more complex anoxic wetland conditions impede decomposition, therefore many wetlands have accumulated large SOM stocks, which is the basis of the global carbon store. When this plant material is still recognizable and accumulates to a certain depth, you have peat There are two major biogeochemical zones in a peatland that critically affect local decomposition processes The upper portion of the peat profile, or the area above the water table, is known as the acrotelm. This area has high O2 concentration, is further aerated by plant roots, recievs the most recent plant litter inputs, has peat that is less decomposed, has more microbial activity, and higher hydraulic conductivity The portion of the peat profile below the water surface is called the catotelm. The proportion of peat entering the catotelm fro m the acrotelm depends on the burial rate and residence time of the litter. Labile C breaks down in the acroteom and the recalcitrant c is what makes it down to the catotelm, so decomposition is inhibited for two reasons below the water table Acrotelm Catotelm

SOM Decomposition in Wetlands Step 1: Depolymerization - Extracellular enzymes cleave large polymers to produce usable monomers that can pass through cell membranes. Both AEROBIC and ANAEROBIC respiration Labile: proteins, carbohydrates, lipids Complex organic polymers Recalcitrant: lignin, hemicellulose Microbially-produced extracellular enzymes Both aerobic and anaerobic decomposition initiated and constrained by cleavage of oranic monomers from large complex organic polymers by exoenzymes - large molecules must be broken down extracellularly Monomers (can pass thru cell membranes) Fatty acids, amino acids, monosaccharides

SOM Decomposition in Wetlands Step 1: Depolymerization - Extracellular enzymes cleave large polymers to produce usable monomers that can pass through cell membranes. Caveat: In ANAEROBIC conditions Oxidative exoenzymes degrade phenolics and lignin Require O2 as an electron acceptor Inhibited by anoxia Contributes to accumulation of recalcitrant material at depth “Enzymatic Latch” phenol oxidases, laccases, and peroxidases that break down recalcitrant C are inhibited in the absence of oxygen, resulting in a build-up of recalcitrant C and limitation of C substrate when oxygen is not available as an electron acceptor (enzymatic latch, Fenner and Freeman 2006). As labile organic material is quickly metabolized in the aerobic portion of the peat profile above the water table, it is these more recalcitrant fractions that resist initial decomposition and are buried, further amplifying SOM accumulation.

SOM Decomposition in Wetlands Step 1: Depolymerization Enzymes!

SOM Decomposition in Wetlands Step 2: Aerobic Respiration “Life is nothing but an electron looking for a place to rest” Albert Szent-Gyorgi (1957) In the presence of oxygen, the small monomers cleaved by exoenzymes (for simplicity, we will say they are now glucose) are oxidized through aerobic cellular respiration. The carbon monomer goes through glycolysis to form two molecules of pyruvate (glycolysis generates 2ATP), which then enter the citric acid cycle and electron transport chain, generating an additional 36 ATP. The oxidized carbon is respired as CO2, with H2O an additional waste product in the reaction.

SOM Decomposition in Wetlands Aerobic Respiration O2 is electron acceptor, reduces organic compounds that are oxidized to CO2 Glucose Pyruvate CH3COCOO- Glycolysis +2 mol ATP Pyruvate dehydrogenase complex In the presence of oxygen, the small monomers cleaved by exoenzymes (for simplicity, we will say they are now glucose) are oxidized through aerobic cellular respiration. The carbon monomer goes through glycolysis to form two molecules of pyruvate (glycolysis generates 2ATP), which then enter the citric acid cycle and electron transport chain, generating an additional 36 ATP. The oxidized carbon is respired as CO2, with H2O an additional waste product in the reaction. Acetyl Co-A CO2 H2O Kreb’s Cycle CO2 +36 mol ATP

SOM Decomposition in Wetlands Step 2: Aerobic Respiration

SOM Decomposition in Wetlands Fermentation In absence of O2, pyruvate degraded to low molecular weight inorganic compounds. Occurs inside the cell, energy is generated by substrate level phosphorylation Glucose/Organic monomers Pyruvate CH3COCOO- Glycolysis +2 mol ATP Fermentation First steps same as aerobic respiration, then fermented to organic acids and alcohols. Fermentation occurs iside the cell and energy is generated by substrate level phosphorylation rather than oxidative phosphorylation by electron transport. Rate determining step for further anaerobic decomposition Extracellular environment Organic acids, acetate, alcohols

SOM Decomposition in Wetlands Fermentation Fermentation breaks down pyruvate into other small organic molecules. The fermentation products become substrates for decomp to CO2 by bacteria using alternitive TEAs. Additional respiratory paths have lower energy yields, so support smaller microbial biomass and lower concentrations of exoenzymes

Lecture 2

SOM Decomposition in Wetlands Aerobic Respiration O2 is electron acceptor, reduces organic compounds that are oxidized to CO2 Glucose Pyruvate CH3COCOO- Glycolysis +2 mol ATP Pyruvate dehydrogenase complex In the presence of oxygen, the small monomers cleaved by exoenzymes (for simplicity, we will say they are now glucose) are oxidized through aerobic cellular respiration. The carbon monomer goes through glycolysis to form two molecules of pyruvate (glycolysis generates 2ATP), which then enter the citric acid cycle and electron transport chain, generating an additional 36 ATP. The oxidized carbon is respired as CO2, with H2O an additional waste product in the reaction. Acetyl Co-A CO2 H2O Kreb’s Cycle CO2 +36 mol ATP C6H12O6 + 6O2 -> 6CO2 + 6H2O dG= -686 kcal/mol

SOM Decomposition in Wetlands Fermentation In absence of O2, pyruvate degraded to low molecular weight inorganic compounds. Occurs inside the cell, energy is generated by substrate level phosphorylation Glucose/Organic monomers Pyruvate CH3COCOO- Glycolysis +2 mol ATP Fermentation First steps same as aerobic respiration, then fermented to organic acids and alcohols. Fermentation occurs iside the cell and energy is generated by substrate level phosphorylation rather than oxidative phosphorylation by electron transport. Rate determining step for further anaerobic decomposition Extracellular environment Organic acids, acetate, alcohols

SOM Decomposition in Wetlands ReDox Chemistry Reduction and Oxidation: the transfer of e- from a donor to an acceptor. One substance is oxidized while another is (in turn) reduced OIL RIG: Oxidation is Loss, Reduction is Gain Plant C the most highly reduced C in the biosphere Standard Reduction Potential (Eo): the tendency of a substance to donate e- and be oxidized or accept e- and be reduced Greater ΔEo, the greater the free energy yield of the reaction (ΔGo) ΔGo = -nFΔE F = Faraday’s constant (23.061 kcal volt-1) n = number of e- The products of fermentation are still reduced compounds that can be oxidized by microbes for additonal energy. Anaerobic respiration is fundamentally redox chemistry, and we will do a quick review so that it makes sense - a reduction-oxidation, or redox, reaction involves the transfer of electrons from a donor to an acceptor. One substance gets oxidized which the other is in turn, reduced - I was taught to remember that OIL RIG - plant carbon is the most highly reduced C in the biosphere, so microbes are going to couple it to a series of redox reactions in order to oxidize the C and gain energy - we think about the standard reduction potential, or the tendency of a substance to donate electrons and be oxidized or accept electrons and be reduced The greater the reduction potential, the greater the free energy yield of the reaction Can calculate the free energy yield of the reaction using faradays constant and the dE

Copyright © 2013 Elsevier Inc. All rights reserved. TABLE 7.3 Common Reduction and Oxidation Half Reactions Copyright © 2013 Elsevier Inc. All rights reserved.

Anaerobic Respiration: Metabolic Pathways SOM Decomposition in Wetlands Anaerobic Respiration: Metabolic Pathways Following O2 depletion, fermentation products are oxidized by series of alternate terminal e- acceptors (TEA) TEA series based on ΔGo of reaction Use substrate-level phosphorylation rather than e- transport chains to produce ATP All pathways yield CO2 Dominance in saturated sediments slows decomposition and C losses Nitrate Reduction/Denitrification Manganese Reduction (often negligible) Iron Reduction Sulfate Reduction ΔGo

SOM Decomposition in Wetlands Nitrate Reduction Most energetically favorable anaerobic C mineralization pathway Performed by facultative anaerobes Zones of fluctuating ReDox (around water table) Precipitation dominated wetlands: [NO3-] low, minor pathway 2NO3- + (CH2O) -> 2N2 + CO2 + H2O ΔG° = -649 kcal/mol Nitrate Reduction/Denitrification Manganese Reduction (often negligible) Iron Reduction Sulfate Reduction ΔGo

SOM Decomposition in Wetlands Nitrate Reduction Fermentation breaks down pyruvate into other small organic molecules. The fermentation products become substrates for decomp to CO2 by bacteria using alternitive TEAs. Additional respiratory paths have lower energy yields, so support smaller microbial biomass and lower concentrations of exoenzymes

SOM Decomposition in Wetlands Manganense Reduction Follows NO3- depletion Mn4+ scarce in wetlands, minor decomposition pathway Spatially overlaps with NO3- zone, performed by facultative anaerobes Nitrate Reduction/Denitrification Manganese Reduction (often negligible) Iron Reduction Sulfate Reduction ΔGo

SOM Decomposition in Wetlands Iron Reduction Follows Mn4+ depletion Below zone of NO3- and Mn4+ depletion Performed by obligate anaerobes Fe(OH)3 + 3H+ -> Fe2+ +3H2O ΔG° = -300 kcal/mol Nitrate Reduction/Denitrification Manganese Reduction (often negligible) Iron Reduction Sulfate Reduction ΔGo

SOM Decomposition in Wetlands Sulfate Reduction Follows Iron depletion Completed by sulfate-reducing bacteria Produce H2S, although H2S fluxes from wetlands are low as it reacts with iron and is sequestered in sediments SO42- + 2(CHO) + 3H+ -> HS- + 2CO2 + 2H2O ΔG° = -190 kcal/mol Nitrate Reduction/Denitrification Manganese Reduction (often negligible) Iron Reduction Sulfate Reduction ΔGo

SOM Decomposition in Wetlands Sulfer Reduction Fermentation breaks down pyruvate into other small organic molecules. The fermentation products become substrates for decomp to CO2 by bacteria using alternitive TEAs. Additional respiratory paths have lower energy yields, so support smaller microbial biomass and lower concentrations of exoenzymes

Methanogenesis Follows depletion of all alternative TEAs Degrade fermentation products and root exudates Performed by Archea Obligatate anaerboes Two methanogenesis pathways: Acetate splitting CH3COOH -> CH4 + CO2 ΔG° = -28 kJ/mol δ13C: -50 to -65 permil CO2 Reduction CO2 + 4H2 -> CH4 + H2O ΔG°= -17.4 kJ/mol δ13C: -60 to -100 permil Assumed acetate, H2, CO2 are three substrates for methanogenesis in freshwater systems. Methylated amines can be substrates in saline systems Patterns in methane release based on availability of TEAs and substrates, all ultimately plant derived. Therefore methen

SOM Decomposition in Wetlands Methanogenesis Fermentation breaks down pyruvate into other small organic molecules. The fermentation products become substrates for decomp to CO2 by bacteria using alternitive TEAs. Additional respiratory paths have lower energy yields, so support smaller microbial biomass and lower concentrations of exoenzymes

Wetland Methane Flux Whiting and Chanton 1993 Precursors to methanogenesis derived from decomposition of C, acetate from decomposition of labile C such as root exudates. Results in strong association between primary production and methane flux. This figure is across wetlands, not peatlands, so get a broad range in NEP. High NPP results in acetoclastic methanogenesis and 13C enrichment Would also expect strong annual cycles in CH4 produciton in these cases Get more acetoclastic at surface and more H2/CO2 at depth, corresponds with more recalcitrant C and further distance from root exudates Whiting and Chanton 1993

CH4 + 2O2 -> CO2 + H2O ΔG° = -193.5 kcal/mol Methane Oxidation Up to 50% of methane produced below WT is oxidized by methanotrophic bacteria in aerobic zone CH4 + 2O2 -> CO2 + H2O ΔG° = -193.5 kcal/mol

SOM Decomposition in Wetlands Methanotrophy Fermentation breaks down pyruvate into other small organic molecules. The fermentation products become substrates for decomp to CO2 by bacteria using alternitive TEAs. Additional respiratory paths have lower energy yields, so support smaller microbial biomass and lower concentrations of exoenzymes

Methane Release to Atmosphere Relationship between NEP and methane flux also due to facilitated gas exchange with wetland plants, aerenchymous tissue are the hollow stems that bring O2 below surface, also transport methane up Ebullition, diffusion, plant transport thru aerenchyma In bogs, methanotrophy limited by low soil bulk density, CH4 ebullates before it has a chance to get oxidized

Steady state methane flux (left) and methane ebullition (right) Demonstrates ebullative flux

Peatlands and Climate Change Changes in state factors: [CO2] -> temperature -> water availability induces physical and biogeochemical changes in the system Plant community dynamics, production, and ecosystem nutrient availability SOM decomposition and nature of greenhouse gas emission

Atmospheric [CO2] Less consistent fertilization effect compared to upland systems Explored in small scale field, mesocosm, lab studies Limited responses due to N limitation (Berendse et al. 2001, Hutchin et al 1995, Hoosbeek et al. 2001, Kang et al. 2001, Saarnio et al. 1998, 2000) Exacerbated N limitation increases root production/exudation Increases dominance of acetoclastic methanogenesis Increased t will increase Increased root production/exudation, increase in acetoclastic methanogenesis

Temperature Increases Permafrost thaw, opens barriers to drainage T results in N mineralization, mediates N limitation SOM decomposition and GG production: Recalcitrant C has higher activation energy, therefore higher temp sensitivity Recalcitrant C turnover more affected by T than labile C Methanogenesis more T sensitive than aerobic respiration

Water table reduction WT reduction increases vascular plant abundance Loss of non-vascular plants -> less recalcitrant SOM -> slower peat accumulation Boreal forest expansion into peatland has net warming effect on radiation balance (Bonan 2008) Peatland expansion onto tundra -> CO2 sink Drier peat-> initial permafrost expansion Sphagnum Lawn ~0-5cm High Water Table ~15-25cm Low Water Table ~40-50cm

Atmospheric Deposition Well studied in European peatlands Increases TEA abundance, decreases methane production (Erikkson and Nilsson 2009) N deposition increases vascular plant abundance relative to Sphagnum Increases decomposition rate due to more recalcitrant litter, ultimately reduces peat accumulation rate

Spruce and Peatland Responses Under Climactic and Environmental Change