Scholarly Work - Land Resources & Environmental Sciences

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    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.
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    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, Bob
    Ice 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.
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    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, Cassidy
    Considerable 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.
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    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.
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    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, Cooper
    The 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.
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    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.
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    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.
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