Scholarly Work - Land Resources & Environmental Sciences
Permanent URI for this collectionhttps://scholarworks.montana.edu/handle/1/8680
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Item Oxic methane production from methylphosphonate in a large oligotrophic lake: limitation by substrate and organic carbon supply(American Society for Microbiology, 2023-11) Peoples, Logan M.; Dore, John E.; Bilbrey, Evan M.; Vick-Majors, Trista J.; Ranieri, John R.; Evans, Kate A.; Ross, Abigail M.; Devlin, Shawn P.; Church, Matthew J.While methane is typically produced under anoxic conditions, methane supersaturation in the presence of oxygen has been observed in both marine and fresh waters. The biological cleavage of methylphosphonate (MPn), which releases both phosphate and methane, is one pathway that may contribute to this paradox. Here, we explore the genomic and functional potential for oxic methane production (OMP) via MPn in Flathead Lake, a large oligotrophic freshwater lake in northwest Montana. Time series and depth profile measurements show that epilimnetic methane was persistently supersaturated despite high oxygen levels, suggesting a possible in situ oxic source. Metagenomic sequencing indicated that 10% of microorganisms in the lake, many of which are related to the Burkholderiales (Betaproteobacteria) and Actinomycetota, have the genomic capacity to cleave MPn. We experimentally demonstrated that these organisms produce methane stoichiometrically with MPn consumption across multiple years. However, methane was only produced at appreciable rates in the presence of MPn when a labile organic carbon source was added, suggesting that this process may be limited by both MPn and labile carbon supply. Members of the genera Acidovorax , Rhodoferax , and Allorhizobium , organisms which make up less than 1% of Flathead Lake communities, consistently responded to MPn addition. We demonstrate that the genomic and physiological potential for MPn use exists among diverse, resident members of Flathead Lake and could contribute to OMP in freshwater lakes when substrates are available. IMPORTANCE Methane is an important greenhouse gas that is typically produced under anoxic conditions. We show that methane is supersaturated in a large oligotrophic lake despite the presence of oxygen. Metagenomic sequencing indicates that diverse, widespread microorganisms may contribute to the oxic production of methane through the cleavage of methylphosphonate. We experimentally demonstrate that these organisms, especially members of the genus Acidovorax , can produce methane through this process. However, appreciable rates of methane production only occurred when both methylphosphonate and labile sources of carbon were added, indicating that this process may be limited to specific niches and may not be completely responsible for methane concentrations in Flathead Lake. This work adds to our understanding of methane dynamics by describing the organisms and the rates at which they can produce methane through an oxic pathway in a representative oligotrophic lake.Item Biogeochemical and historical drivers of microbial community composition and structure in sediments from Mercer Subglacial Lake, West Antarctica(Springer Science and Business Media LLC, 2023-01) Davis, Christina L.; Venturelli, Ryan A.; Michaud, Alexander B.; Hawkings, Jon R.; Achberger, Amanda M.; Vick-Majors, Trista J.; Rosenheim, Brad E.; Dore, John E.; Steigmeyer, August; Skidmore, Mark L.; Barker, Joel D.; Benning, Liane G.; Siegfried, Matthew R.; Priscu, John C.; Christner, Brent C.; Barbante, Carlo; Bowling, Mark; Burnett, Justin; Campbell, Timothy; Collins, Billy; Dean, Cindy; Duling, Dennis; Fricker, Helen A.; Gagnon, Alan; Gardner, Christopher; Gibson, Dar; Gustafson, Chloe; Harwood, David; Kalin, Jonas; Kasic, Kathy; Kim, Ok-Sun; Krula, Edwin; Leventer, Amy; Li, Wei; Lyons, W. Berry; McGill, Patrick; McManis, James; McPike, David; Mironov, Anatoly; Patterson, Molly; Roberts, Graham; Rot, James; Trainor, Cathy; Tranter, Martyn; Winans, John; Zook, BobIce streams that flow into Ross Ice Shelf are underlain by water-saturated sediments, a dynamic hydrological system, and subglacial lakes that intermittently discharge water downstream across grounding zones of West Antarctic Ice Sheet (WAIS). A 2.06 m composite sediment profile was recently recovered from Mercer Subglacial Lake, a 15 m deep water cavity beneath a 1087 m thick portion of the Mercer Ice Stream. We examined microbial abundances, used 16S rRNA gene amplicon sequencing to assess community structures, and characterized extracellular polymeric substances (EPS) associated with distinct lithologic units in the sediments. Bacterial and archaeal communities in the surficial sediments are more abundant and diverse, with significantly different compositions from those found deeper in the sediment column. The most abundant taxa are related to chemolithoautotrophs capable of oxidizing reduced nitrogen, sulfur, and iron compounds with oxygen, nitrate, or iron. Concentrations of dissolved methane and total organic carbon together with water content in the sediments are the strongest predictors of taxon and community composition. δ¹³C values for EPS (−25 to −30‰) are consistent with the primary source of carbon for biosynthesis originating from legacy marine organic matter. Comparison of communities to those in lake sediments under an adjacent ice stream (Whillans Subglacial Lake) and near its grounding zone provide seminal evidence for a subglacial metacommunity that is biogeochemically and evolutionarily linked through ice sheet dynamics and the transport of microbes, water, and sediments beneath WAIS.Item Sustained stoichiometric imbalance and its ecological consequences in a large oligotrophic lake(Proceedings of the National Academy of Sciences, 2022-07) Elser, James J.; Devlin, Shawn P.; Yu, Jinlei; Baumann, Adam; Church, Matthew J.; Dore, John E.; Hall, Robert O.; Hollar, Melody; Johnson, Tyler; Vick-Majors, Trista; White, CassidyConsiderable attention is given to absolute nutrient levels in lakes, rivers, and oceans, but less is paid to their relative concentrations, their nitrogen:phosphorus (N:P) stoichiometry, and the consequences of imbalanced stoichiometry. Here, we report 38 y of nutrient dynamics in Flathead Lake, a large oligotrophic lake in Montana, and its inflows. While nutrient levels were low, the lake had sustained high total N: total P ratios (TN:TP: 60 to 90:1 molar) throughout the observation period. N and P loading to the lake as well as loading N:P ratios varied considerably among years but showed no systematic long-term trend. Surprisingly, TN:TP ratios in river inflows were consistently lower than in the lake, suggesting that forms of P in riverine loading are removed preferentially to N. In-lake processes, such as differential sedimentation of P relative to N or accumulation of fixed N in excess of denitrification, likely also operate to maintain the lake’s high TN:TP ratios. Regardless of causes, the lake’s stoichiometric imbalance is manifested in P limitation of phytoplankton growth during early and midsummer, resulting in high C:P and N:P ratios in suspended particulate matter that propagate P limitation to zooplankton. Finally, the lake’s imbalanced N:P stoichiometry appears to raise the potential for aerobic methane production via metabolism of phosphonate compounds by P-limited microbes. These data highlight the importance of not only absolute N and P levels in aquatic ecosystems, but also their stoichiometric balance, and they call attention to potential management implications of high N:P ratios.Item Aerobic bacterial methane synthesis(Proceedings of the National Academy of Sciences, 2021-06) Wang, Qian; Alowaifeer, Abdullah; Kerner, Patricia; Balasubramanian, Narayanaganesh; Patterson, Angela; Christian, William; Tarver, Angela; Dore, John E.; Hatzenpichler, Roland; Bothner, Brian; McDermott, Timothy R.Reports of biogenic methane (CH4) synthesis associated with a range of organisms have steadily accumulated in the literature. This has not happened without controversy and in most cases the process is poorly understood at the gene and enzyme levels. In marine and freshwater environments, CH4 supersaturation of oxic surface waters has been termed the “methane paradox” because biological CH4 synthesis is viewed to be a strictly anaerobic process carried out by O2-sensitive methanogens. Interest in this phenomenon has surged within the past decade because of the importance of understanding sources and sinks of this potent greenhouse gas. In our work on Yellowstone Lake in Yellowstone National Park, we demonstrate microbiological conversion of methylamine to CH4 and isolate and characterize an Acidovorax sp. capable of this activity. Furthermore, we identify and clone a gene critical to this process (encodes pyridoxylamine phosphate-dependent aspartate aminotransferase) and demonstrate that this property can be transferred to Escherichia coli with this gene and will occur as a purified enzyme. This previously unrecognized process sheds light on environmental cycling of CH4, suggesting that O2-insensitive, ecologically relevant aerobic CH4 synthesis is likely of widespread distribution in the environment and should be considered in CH4 modeling efforts.Item Scientific access into Mercer Subglacial Lake: scientific objectives, drilling operations and initial observations(Cambridge University Press, 2021-06) Priscu, John C.; Kalin, Jonas; Winans, John; Campbell, Timothy; Siegfried, Matthew R.; Skidmore, Mark; Dore, John E.; Leventer, Amy; Harwood, David M.; Duling, Dennis; Zook, Robert; Burnett, Justin; Gibson, Dar; Krula, Edward; Mironov, Anatoly; McManis, Jim; Roberts, Graham; Rosenheim, Brad E.; Christner, Brent C.; Kasic, Kathy; Fricker, Helen A.; Lyons, W. Berry; Barker, Joel; Bowling, Mark; Collings, Billy; Davis, Christina; Gagnon, Al; Gardner, Christopher; Gustafson, Chloe; Kim, Ok-Sun; Li, Wei; Michaud, Alex; Patterson, Molly O.; Tranter, Martyn; Venturelli, Ryan; Vick-Majors, Trista; Elsworth, CooperThe Subglacial Antarctic Lakes Scientific Access (SALSA) Project accessed Mercer Subglacial Lake using environmentally clean hot-water drilling to examine interactions among ice, water, sediment, rock, microbes and carbon reservoirs within the lake water column and underlying sediments. A ~0.4 m diameter borehole was melted through 1087 m of ice and maintained over ~10 days, allowing observation of ice properties and collection of water and sediment with various tools. Over this period, SALSA collected: 60 L of lake water and 10 L of deep borehole water; microbes >0.2 μm in diameter from in situ filtration of ~100 L of lake water; 10 multicores 0.32–0.49 m long; 1.0 and 1.76 m long gravity cores; three conductivity–temperature–depth profiles of borehole and lake water; five discrete depth current meter measurements in the lake and images of ice, the lake water–ice interface and lake sediments. Temperature and conductivity data showed the hydrodynamic character of water mixing between the borehole and lake after entry. Models simulating melting of the ~6 m thick basal accreted ice layer imply that debris fall-out through the ~15 m water column to the lake sediments from borehole melting had little effect on the stratigraphy of surficial sediment cores.Item Seasonal-to-decadal scale variability in primary production and particulate matter export at Station ALOHA(2021-07) Karl, David M.; Letelier, Ricardo M.; Bidigare, Robert R.; Bjorkman, Karin M.; Church, Matthew J.; Dore, John E.; White, Angelicque E.Station ALOHA (A Long-term Oligotrophic Habitat Assessment) was established in the North Pacific Subtropical Gyre (22°45′N, 158°W) as an oligotrophic ocean benchmark to improve our understanding of processes that govern the fluxes of carbon (C) into and from the surface ocean. At approximately monthly intervals, measurements of the primary production of particulate C (PC) using the 14C method, and the export of PC and particulate nitrogen (PN) using surface-tethered sediment traps deployed at 150 m have been made along with a host of complementary physical, biological, and biogeochemical measurements. Euphotic zone depth-integrated (0–200 m) primary production ranged from 220.2 (standard deviation, SD, 10.8) mg C m−2 d−1 in Feb 2018 to 1136.5 (SD = 17.1) mg C m−2 d−1 in Jun 2000, with a 30-yr (1989–2018) mean of 536.8 (SD = 135.0) mg C m−2 d−1 (n = 271). Although the monthly primary production climatology was fairly well constrained, we observed substantial sub-decadal variability and a significant 0–125 m depth-integrated increasing trend of 4.0 (p < 0.01; 95% confidence interval, CI, 2.1–5.9) (mg C m−2 d−1) yr−1 since 1989, displaying a large relative increase of 37% (CI = 18–55%) in the lower portion (75–125 m) of the euphotic zone. Chlorophyll (Chl) a and suspended PC and PN concentrations also displayed significant (p < 0.01) increases in the 75–125 m region of the euphotic zone. PC export at 150 m exhibited both short-term (monthly) and longer-scale variability with a 30-yr mean of 27.9 (SD = 9.7, n = 265) mg C m−2 d−1. PC and PN export exhibited extended, multi-year periods of significantly lower or higher values compared to the 30-yr mean. These multi-year periods of anomalously low and high particle export, in the absence of contemporaneous variations in primary production, probably reflect periodic changes in remineralization efficiencies. The PC export ratio (e-ratio; PC export at 150 m ÷ 0–150 m depth-integrated 14C-based primary production) was low, with a 30-yr mean of 0.054 (SD = 0.021, n = 248), and exhibited a significant (p < 0.01) long-term decreasing trend over the 30-yr observation period. The 30-yr long-term increases in primary production (~37%), Chl a, and suspended PC and PN concentrations (~17%, 8%, and 8%, respectively) in the 75–125 m portion of the water column are hypothesized to result from an enhanced supply of nutrients to the lower portion of the water column over the past three decades.Item Biogeochemical Connectivity Between Freshwater Ecosystems beneath the West Antarctic Ice Sheet and the Sub‐Ice Marine Environment(2020-03) Vick‐Majors, Trista J.; Michaud, Alexander B.; Skidmore, Mark L.; Turetta, Clara; Barbante, Carlo; Christner, Brent C.; Dore, John E.; Christianson, Knut; Mitchell, Andrew C.; Achberger, Amanda M.; Mikucki, Jill A.; Priscu, John C.Although subglacial aquatic environments are widespread beneath the Antarctic ice sheet, subglacial biogeochemistry is not well understood, and the contribution of subglacial water to coastal ocean carbon and nutrient cycling remains poorly constrained. The Whillans Subglacial Lake (SLW) ecosystem is upstream from West Antarctica's Gould‐Siple Coast ~800 m beneath the surface of the Whillans Ice Stream. SLW hosts an active microbial ecosystem and is part of an active hydrological system that drains into the marine cavity beneath the adjacent Ross Ice Shelf. Here we examine sources and sinks for organic matter in the lake and estimate the freshwater carbon and nutrient delivery from discharges into the coastal embayment. Fluorescence‐based characterization of dissolved organic matter revealed microbially driven differences between sediment pore waters and lake water, with an increasing contribution from relict humic‐like dissolved organic matter with sediment depth. Mass balance calculations indicated that the pool of dissolved organic carbon in the SLW water column could be produced in 4.8 to 11.9 yr, which is a time frame similar to that of the lakes’ fill‐drain cycle. Based on these estimates, subglacial lake water discharged at the Siple Coast could supply an average of 5,400% more than the heterotrophic carbon demand within Siple Coast embayments (6.5% for the entire Ross Ice Shelf cavity). Our results suggest that subglacial discharge represents a heretofore unappreciated source of microbially processed dissolved organic carbon and other nutrients to the Southern Ocean.Item Landscape analysis of soil methane flux across complex terrain(2018-05) Kaiser, Kendra E.; McGlynn, Brian L.; Dore, John E.Relationships between methane (CH4) fluxes and environmental conditions have been extensively explored in saturated soils, while research has been less prevalent in aerated soils because of the relatively small magnitudes of CH4 fluxes that occur in dry soils. Our study builds on previous carbon cycle research at Tenderfoot Creek Experimental Forest, Montana, to identify how environmental conditions reflected by topographic metrics can be leveraged to estimate watershed scale CH4 fluxes from point scale measurements. Here, we measured soil CH4 concentrations and fluxes across a range of landscape positions (7 riparian, 25 upland), utilizing topographic and seasonal (29 May-12 September) gradients to examine the relationships between environmental variables, hydrologic dynamics, and CH4 emission and uptake. Riparian areas emitted small fluxes of CH4 throughout the study (median: 0.186 mu g CH4-Cm-2 h(-1)) and uplands increased in sink strength with dry-down of the watershed (median: -22.9 mu g CH4-Cm-2 h(-1)). Locations with volumetric water content (VWC) below 38% were methane sinks, and uptake increased with decreasing VWC. Above 43% VWC, net CH4 efflux occurred, and at intermediate VWC net fluxes were near zero. Riparian sites had near-neutral cumulative seasonal flux, and cumulative uptake of CH4 in the uplands was significantly related to topographic indices. These relationships were used to model the net seasonal CH4 flux of the upper Stringer Creek watershed (-1.75 kg CH4-Cha(-1)). This spatially distributed estimate was 111% larger than that obtained by simply extrapolating the mean CH4 flux to the entire watershed area. Our results highlight the importance of quantifying the space-time variability of net CH4 fluxes as predicted by the frequency distri- bution of landscape positions when assessing watershed scale greenhouse gas balances.Item Microbial oxidation as a methane sink beneath the West Antarctic Ice Sheet(2017-07) Michaud, Alexander B.; Dore, John E.; Achberger, Amanda M.; Christner, Brent C.; Mitchell, Andrew C.; Skidmore, Mark L.; Vick-Majors, Trista J.; Priscu, John C.Aquatic habitats beneath ice masses contain active microbial ecosystems capable of cycling important greenhouse gases, such as methane (CH4). A large methane reservoir is thought to exist beneath the West Antarctic Ice Sheet, but its quantity, source and ultimate fate are poorly understood. For instance, O2 supplied by basal melting should result in conditions favourable for aerobic methane oxidation. Here we use measurements of methane concentrations and stable isotope compositions along with genomic analyses to assess the sources and cycling of methane in Subglacial Lake Whillans (SLW) in West Antarctica. We show that sub-ice-sheet methane is produced through the biological reduction of CO2 using H2. This methane pool is subsequently consumed by aerobic, bacterial methane oxidation at the SLW sediment–water interface. Bacterial oxidation consumes >99% of the methane and represents a significant methane sink, and source of biomass carbon and metabolic energy to the surficial SLW sediments. We conclude that aerobic methanotrophy may mitigate the release of methane to the atmosphere upon subglacial water drainage to ice sheet margins and during periods of deglaciation.Item Physiological Ecology of Microorganisms in Subglacial Lake Whillans(2016-10) Vick-Majors, Trista J.; Mitchell, Andrew C.; Achberger, Amanda M.; Christner, Brent C.; Dore, John E.; Michaud, Alexander B.; Mikucki, Jill A.; Purcell, Alicia M.; Skidmore, Mark L.; Priscu, John C.Subglacial microbial habitats are widespread in glaciated regions of our planet. Some of these environments have been isolated from the atmosphere and from sunlight for many thousands of years. Consequently, ecosystem processes must rely on energy gained from the oxidation of inorganic substrates or detrital organic matter. Subglacial Lake Whillans (SLW) is one of more than 400 subglacial lakes known to exist under the Antarctic ice sheet; however, little is known about microbial physiology and energetics in these systems. When it was sampled through its 800 m thick ice cover in 2013, the SLW water column was shallow (~2 m deep), oxygenated, and possessed sufficient concentrations of C, N, and P substrates to support microbial growth. Here, we use a combination of physiological assays and models to assess the energetics of microbial life in SLW. In general, SLW microorganisms grew slowly in this energy-limited environment. Heterotrophic cellular carbon turnover times, calculated from (3)H-thymidine and (3)H-leucine incorporation rates, were long (60 to 500 days) while cellular doubling times averaged 196 days. Inferred growth rates (average ~0.006 d(-1)) obtained from the same incubations were at least an order of magnitude lower than those measured in Antarctic surface lakes and oligotrophic areas of the ocean. Low growth efficiency (8%) indicated that heterotrophic populations in SLW partition a majority of their carbon demand to cellular maintenance rather than growth. Chemoautotrophic CO2-fixation exceeded heterotrophic organic C-demand by a factor of ~1.5. Aerobic respiratory activity associated with heterotrophic and chemoautotrophic metabolism surpassed the estimated supply of oxygen to SLW, implying that microbial activity could deplete the oxygenated waters, resulting in anoxia. We used thermodynamic calculations to examine the biogeochemical and energetic consequences of environmentally imposed switching between aerobic and anaerobic metabolisms in the SLW water column. Heterotrophic metabolisms utilizing acetate and formate as electron donors yielded less energy than chemolithotrophic metabolisms when calculated in terms of energy density, which supports experimental results that showed chemoautotrophic activity in excess of heterotrophic activity. The microbial communities of subglacial lake ecosystems provide important natural laboratories to study the physiological and biogeochemical behavior of microorganisms inhabiting cold, dark environments.