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Inorganic carbon fixation in ice-covered lakes of the McMurdo Dry Valleys

Published online by Cambridge University Press:  03 April 2019

Trista J. Vick-Majors
Affiliation:
Department of Land Resources and Environmental Sciences, Montana State University, 334 Leon Johnson Hall, Bozeman, MT 59717, USA
John C. Priscu*
Affiliation:
Department of Land Resources and Environmental Sciences, Montana State University, 334 Leon Johnson Hall, Bozeman, MT 59717, USA

Abstract

Inorganic carbon fixation, usually mediated by photosynthetic microorganisms, is considered to form the base of the food chain in aquatic ecosystems. In high-latitude lakes, lack of sunlight owing to seasonal solar radiation limits the activity of photosynthetic plankton during the polar winter, causing respiration-driven demand for carbon to exceed supply. Here, we show that inorganic carbon fixation in the dark, driven by organisms that gain energy from chemical reactions rather than sunlight (chemolithoautotrophs), provides a significant influx of fixed carbon to two permanently ice-covered lakes (Fryxell and East Bonney). Fryxell, which has higher biomass per unit volume of water, had higher rates of inorganic dark carbon fixation by chemolithoautotrophs than East Bonney (trophogenic zone average 1.0 µg C l−1 d−1vs 0.08 µg C l−1 d−1, respectively). This contribution from dark carbon fixation was partly due to the activity of ammonia oxidizers, which are present in both lakes. Despite the potential importance of new carbon input by chemolithoautotrophic activity, both lakes remain net heterotrophic, with respiratory demand for carbon exceeding supply. Dark carbon fixation increased the ratio of new carbon supply to respiratory demand from 0.16 to 0.47 in Fryxell, and from 0.14 to 0.22 in East Bonney.

Type
Biological Sciences
Copyright
Copyright © Antarctic Science Ltd 2019 

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Footnotes

*

Present address: Flathead Lake Biological Station, University of Montana, 32125 Bio Station Lane, Polson, MT 59860, USA

References

Bielewicz, S., Bell, E., Kong, W., Friedberg, I., Priscu, J.C. & Morgan-Kiss, R.M. 2011. Protist diversity in a permanently ice-covered Antarctic lake during the polar night transition. The ISME Journal, 5, 10.1038/ismej.2011.23.Google Scholar
Bowman, J.S., Vick-Majors, T.J., Morgan-Kiss, R., Takacs-Vesbach, C., Ducklow, H.W. & Priscu, J.C. 2016. Microbial community dynamics in two polar extremes: the lakes of the McMurdo Dry Valleys and the West Antarctic Peninsula marine ecosystem. Bioscience, 66, 10.1093/biosci/biw103.Google Scholar
Dolhi, J.M., Teufel, A.G., Kong, W. & Morgan-Kiss, R.M. 2015. Diversity and spatial distribution of autotrophic communities within and between ice-covered Antarctic lakes (McMurdo Dry Valleys). Limnology and Oceanography, 60, 10.1002/lno.10071.Google Scholar
Dore, J.E. & Priscu, J.C. 2001. Phytoplankton phosphorus deficiency and alkaline phosphatase activity in the McMurdo Dry Valley lakes, Antarctica. Limnology and Oceanography, 46, 13311346.Google Scholar
Gooseff, M.N., Barrett, J.E., Adams, B.J., Doran, P.T., Fountain, A.G., Lyons, W.B., et al. 2017. Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica. Nature Ecology & Evolution, 1, 10.1038/s41559-017-0253-0.Google Scholar
Hawes, I., Moorhead, D., Sutherland, D., Schmeling, J. & Schwarx, A.M. 2001. Benthic primary production in two perennially ice-covered Antarctic lakes: patterns of biomass accumulation with a model of community metabolism. Antarctic Science, 13, 10.1017/S0954102001000049Google Scholar
Jäntti, H., Jokinen, S., Hietanen, S., Jokinen, S. & Hietanen, S. 2013. Effect of nitrification inhibitors on the Baltic Sea ammonia-oxidizing community and precision of the denitrifier method. Aquatic Microbial Ecology, 70, 10.3354/ame01653.Google Scholar
Joye, S.B., Connell, T.L., Miller, L.G., Oremland, R.S. & Jellison, R.S. 1999. Oxidation of ammonia and methane in an alkaline, saline lake. Limnology and Oceanography, 1, 10.4319/lo.1999.44.1.0178.Google Scholar
Jungblut, A.D., Hawes, I., Mackey, T.J., Krusor, M., Doran, P.T., Sumner, D.Y., et al. 2016. Microbial mat communities along an oxygen gradient in a perennially ice-covered Antarctic lake. Applied and Environmental Microbiology, 82, 10.1128/AEM.02699-15.Google Scholar
Karr, E.A., Ng, J.M., Belchik, S.M. & Sattley, W.M. 2006. Biodiversity of methanogenic and other Archaea in the permanently frozen Lake Fryxell, Antarctica. Applied and Environmental Microbiology, 72, 10.1128/AEM.72.2.1663.Google Scholar
Karr, E.A., Sattley, W.M., Jung, D.O., Madigan, M.T. & Achenbach, L.A. 2003. Remarkable diversity of phototrophic purple bacteria in a permanently frozen Antarctic lake. Applied and Environmental Microbiology, 69, 10.1128/AEM.69.8.4910-4914.2003.Google Scholar
Kong, W., Ream, D.C., Priscu, J.C. & Morgan-Kiss, R.M. 2012. Diversity and expression of RubisCO genes in a perennially ice-covered Antarctic lake during the polar night transition. Applied and Environmental Microbiology, 78, 10.1128/AEM.00029-12.Google Scholar
Laybourn-Parry, J., James, M.R., McKnight, D.M., Priscu, J., Spaulding, S.A. & Shiel, R. 1997. The microbial plankton of Lake Fryxell, southern Victoria Land, Antarctica during the summers of 1992 and 1994. Polar Biology, 17, 10.1007/s003000050104.Google Scholar
Lizotte, M.P. & Priscu, J.C. 1992. Spectral irradiance and bio-optical properties in perennially ice-covered lakes of the dry valleys (McMurdo Sound, Antarctica). Antarctic Research Series, 57, 10.1029/ar057p0001.Google Scholar
Lizotte, M.P., Sharp, T.R. & Priscu, J.C. 1996. Phytoplankton dynamics in the stratified water column of Lake Bonney, Antarctica. Polar Biology, 16, 10.1007/bf02329203.Google Scholar
Madigan, M.T. 2009. The purple phototrophic bacteria. In Hunter, C.N., Daldal, F., Thurnauer, M.C. & Beatty, J.T., eds. Advances in photosynthesis and respiration. Dordrecht: Springer, 1013 pp.Google Scholar
McKnight, D.M., Howes, B.L. & Taylor, C.D. 2000. Phytoplankton dynamics in a stably stratified Antarctic lake during winter darkness. Journal of Phycology, 36, 10.1046/j.1529-8817.2000.00031.x.Google Scholar
Moorhead, D., Schmeling, J. & Hawes, I. 2005. Modelling the contribution of benthic microbial mats to net primary production in Lake Hoare, McMurdo Dry Valleys. Antarctic Science, 17, 10.1017/S0954102005002403.Google Scholar
Morana, C., Roland, F.A.E., Crowe, S.A., Llirós, M., Borges, A.V., Darchambeau, F. & Bouillon, S. 2016. Chemoautotrophy and anoxygenic photosynthesis within the water column of a large meromictic tropical lake (Lake Kivu, East Africa). Limnology and Oceanography, 61, 10.1002/lno.10304.Google Scholar
Morgan-Kiss, R.M., Lizotte, M.P., Kong, W. & Priscu, J.C. 2015. Photoadaptation to the polar night by phytoplankton in a permanently ice-covered Antarctic lake. Limnology and Oceanography, 61, 10.1002/lno.10107.Google Scholar
Parker, B.C., Simmons, G.M, Wharton, R.A., Seaburg, K.G. & Love, F.G. 1982. Removal of organic and inorganic matter from Antarctic lakes by aerial escape of blue-green algal mats. Journal of Phycology, 18, 7278.Google Scholar
Pouliot, J., Galand, P.E., Lovejoy, C. & Vincent, W.F. 2009. Vertical structure of archaeal communities and distribution of ammonia monooxygenase A gene variants in two meromictic High Arctic lakes. Environmental Microbiology, 11, 687699.Google Scholar
Priscu, J.C., Downes, M.T. & McKay, C.P. 1996. Extreme supersaturation of nitrous oxide in a poorly ventilated Antarctic lake. Limnology and Oceanography, 41, 15441551.Google Scholar
Priscu, J.C., Priscu, L.R., Howard-Williams, C. & Vincent, W.F. 1988. Diel patterns of photosynthate biosynthesis by phytoplankton in permanently ice-covered Antarctic lakes under continuous sunlight. Journal of Plankton Research, 10, 10.1093/plankt/10.3.333.Google Scholar
Priscu, J.C., Priscu, L.R., Vincent, W.F. & Howard-Williams, C. 1987. Photosynthate distribution by microplankton in permanently ice-covered Antarctic desert lakes. Limnology and Oceanography, 32, 10.4319/lo.1987.32.1.0260.Google Scholar
Priscu, J.C., Christner, B.C., Dore, J.E., Westley, M.B., Popp, B.N., Casciotti, K.L. & Lyons, W.B. 2008. Extremely supersaturated N2O in a perennially ice-covered Antarctic lake: molecular and stable isotopic evidence for a biogeochemical relict. Limnology and Oceanography, 53, 24392450.Google Scholar
Priscu, J. & Schmok, J. 2014. McMurdo Dry Valleys bathymetric values from contour map digitizing. Environmental Data Initiative. http://dx.doi.org/10.6073/pasta/dacf78e180d518ddfd52efd7c111b8e1 (accessed 23 February 2019).Google Scholar
Priscu, J.C., Wolf, C.F. & Takacs, C.D. 1999. Carbon transformations in a perennially ice-covered Antarctic lake. Bioscience, 49, 10.2307/1313733.Google Scholar
Roberts, E.C., Priscu, J.C., Wolf, C., Lyons, W.B. & Laybourn-Parry, J. 2004. The distribution of microplankton in the McMurdo Dry Valley lakes, Antarctica: response to ecosystem legacy or present-day climatic controls? Polar Biology, 27, 10.1007/s00300-003-0582-0.Google Scholar
Sattley, W.M. & Madigan, M.T. 2006. Isolation, characterization, and ecology of cold-active, chemolithotrophic, sulfur-oxidizing bacteria from perennially ice-covered Lake Fryxell, Antarctica. Applied and Environmental Microbiology, 72, 10.1128/AEM.00702-06.Google Scholar
Saxton, M.A., Samarkin, V.A., Schutte, C.A., Bowles, M.W., Madigan, M.T., Cadieux, S.B., et al. 2016. Biogeochemical and 16S rRNA gene sequence evidence supports a novel mode of anaerobic methanotrophy in permanently ice-covered Lake Fryxell, Antarctica. Limnology and Oceanography, 61, 10.1002/lno.10320.Google Scholar
Sharp, T.R. 1993. Temporal and spatial variation of light, nutrients, and phytoplankton production in Lake Bonney, Antarctica. MSc thesis, Montana State University, 183 pp [Unpublished].Google Scholar
Spigel, R.H. & Priscu, J.C. 1998. Physical limnology of the McMurdo Dry Valleys lakes. Antarctic Research Series, 72, 153187.Google Scholar
Takacs, C. & Priscu, J. 1998. Bacterioplankton dynamics in the McMurdo Dry Valley lakes, Antarctica: production and biomass loss over four seasons. Microbial Ecology, 36, 239250.Google Scholar
Takacs, C.D., Priscu, J.C. & McKnight, D.M. 2001. Bacterial dissolved organic carbon demand in McMurdo Dry Valley lakes, Antarctica. Limnology and Oceanography, 46, 11891194.Google Scholar
Topp, E. & Knowles, R. 1982. Nitrapyrin inhibits the obligate methylotrophs Methylosinus trichosporium and Methylococcus capsulatus. FEMS Microbiology Letters, 14, 4749.Google Scholar
Vick, T.J. & Priscu, J.C. 2012. Bacterioplankton productivity in lakes of the Taylor Valley, Antarctica, during the polar night transition. Aquatic Microbial Ecology, 68, 10.3354/ame01604.Google Scholar
Vick-Majors, T.J., Priscu, J.C. & Amaral-Zettler, L.A. 2014. Modular community structure suggests metabolic plasticity during the transition to polar night in ice-covered Antarctic lakes. The ISME Journal, 8, 10.1038/ismej.2013.190.Google Scholar
Vincent, W.F. 1981. Production strategies in Antarctic inland waters: phytoplankton eco-physiology in a permanently ice-covered lake. Ecology, 62, 10.2307/1937286.Google Scholar
Voytek, M.A., Priscu, J.C. & Ward, B.B. 1999. The distribution and relative abundance of ammonia-oxidizing bacteria in lakes of the McMurdo Dry Valleys, Antarctica. Hydrobiologia, 401, 10.1007/978-94-011-4201-4_9.Google Scholar