Robert Michael McKay
Microbes promote ice formation in large lakes
Whereas sea ice supports diverse and productive assemblages of planktonic microbes in polar waters, only limited information is available on the sympagic habitat in freshwater ecosystems. We recently presented evidence for the cooperation of phytoplankton and epiphytic bacteria to engineer their environment by the directed formation of ice in a freshwater ecosystem. Annual winter surveys of Lake Erie, one of the Laurentian Great Lakes, reveal ice nucleation activity associated with assemblages of filamentous diatoms sampled from the ice-covered lake. We posit that these non-motile phytoplankton exploit the ability to promote ice formation to attach to overlying ice and thereby maintain a favorable position in the photic zone. However, it is unlikely that the diatoms themselves promote ice nucleation. Rather, we attribute the ice nucleation activity to bacteria; scanning electron microscopy revealed associations of bacterial epiphytes with the dominant diatoms of the phytoplankton assemblage and bacteria isolated from the phytoplankton showed high temperatures of crystallization (Tc) to -3°C. Ice nucleation-active (INA) isolates were identified as belonging to the genus Pseudomonas. Whereas their presence in lakes has been attributed to environmental runoff and atmospheric deposition consistent with their role as biological ice nuclei in clouds, recent data support the existence of an aquatic clade. Far from a passive existence in the aquatic milieu, the INA microbes associated with winter diatom assemblages possess a role in ice formation, which in turn promotes the growth of their diatom hosts. This novel cooperative mechanism illuminates a previously-undescribed stage of the life cycle of pseudomonads in the environment, and offers a model of mutualism relevant to aquatic ecosystems having seasonal ice cover around the world.
We continue to survey the distribution (spatial and temporal) of ice nucleating activity among the Laurentian Great Lakes and other large lakes. We will also characterize ice nucleation activity in the Great Lakes to identify physico-chemical factors that influence the environmental expression of the ice nucleation phenotype. Our efforts will also focus on characterizing the diversity of ice nucleation-active microbes in the Laurentian Great Lakes and will examine the ecological implications of this bacterial-phytoplankton association.
Steffen, M.M., T.W. Davis, R.M. McKay, G.S. Bullerjahn, L.E. Krausfeldt, J.M.A. Stough, M.L. Neitzey, N.E. Gilbert, G.L. Boyer, T.H. Johengen, D.C. Gossiaux, A.M. Burtner, D. Palladino, M. Rowe, G.J. Dick, K. Meyer, S. Levy, B. Boone, R. Stumpf, T. Wynne, P.V. Zimba, D.B. Gutierrez, S.W. Wilhelm. 2017. Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: Linkages between biology and the water supply shutdown of Toledo, Ohio. Environmental Science & Technology, 51: 6745-6755.
Hampton, S.E., A.W.E. Galloway, S.M. Powers, T. Ozersky, K.H. Woo, R.D. Batt, S.G. Labou, C.M. O’Reilly, S. Sharma, N.R. Lottig, E.H. Stanley, R.L. North, J.D. Stockwell, R. Adrian, G.A. Weyhenmeyer, L. Arvola, H.M. Baulch, I. Bertani, L.L. Bowman, Jr., C.C. Carey, J. Catalan, W. Colom-Montero, L.M. Domine, M. Felip, I. Granados, C. Gries, H.-P. Grossart, J. Haberman, M. Haldna, B. Hayden, S.N. Higgins, J.C. Jolley, K.K. Kahilainen, E. Kaup, M.J. Kehoe, S. MacIntyre, A.W. Mackay, H.L. Mariash, R.M. McKay, B. Nixdorf, P. Nõges, T. Nõges, M. Palmer, D.C. Pierson, D.M. Post, M.J. Pruett, M. Rautio, J.S. Read, S.L. Roberts, J. Rücker, S. Sadro, E.A. Silow, D.E. Smith, R.W. Sterner, G.E.A. Swann, M.A. Timofeyev, M. Toro, M.R. Twiss, R.J. Vogt, S.B. Watson, E.J. Whiteford, and M.A. Xenopoulos. 2017. Ecology under lake ice. Ecology Letters 20: 98-111.
Bullerjahn, G.S., R.M.L. McKay, T.W. Davis, D.B. Baker, G.L. Boyer, L.V. D’Anglada, G.J. Doucette, J.C. Ho, E.G. Irwin, C.L. Kling, R.M. Kudela, R. Kurmayer, A.M. Michalak, J.D. Ortiz, T.G. Otten, H.W. Paerl, B. Qin, B.L. Sohngen, R.P. Stumpf, P.M. Visser, and S.W. Wilhelm. 2016. Global solutions to regional problems: Collecting global expertise to address the problem of harmful cyanobacterial blooms. A Lake Erie case study. Harmful Algae 54: 223-238.
Beall, B.F.N., M.R. Twiss, D. Smith, B. Oyserman, M.J. Rozmarynowycz, C. Binding, R.A. Bourbonniere, G.S. Bullerjahn, M. Palmer, E.D. Reavie, M.K. Waters, W.C. Woityra, and R.M.L. McKay. 2016. Ice cover extent drives phytoplankton- and bacterial community structure in a large north-temperate lake: Implications for a warming climate. Environmental Microbiology 18: 1704–1719. (selected for journal cover image)
Beall, B.F.N., M.R. Twiss, D. Smith, B. Oyserman, M.J. Rozmarynowycz, C. Binding, R.A. Bourbonniere, G.S. Bullerjahn, M. Palmer, E.D. Reavie, M.K. Waters, W.C. Woityra, and R.M.L. McKay. 2016. Ice cover extent drives phytoplankton- and bacterial community structure in a large north-temperate lake: Implications for a warming climate. Environmental Microbiology doi: 10.1111/1462-2920.12819
McKay, R.M.L., O. Prášil, L. Pechar, E. Lawrenz, MJ. Rozmarynowycz, and G.S. Bullerjahn. 2015. Freshwater ice as habitat: Partitioning of phytoplankton- and bacteria between ice and water in central European reservoirs. Environmental Microbiology Reports 7: 887-898.
Wilhelm, S.W., G.R. LeClair, G.S. Bullerjahn, R.M. McKay, M.A. Saxton, M.R. Twiss, and R.A. Bourbonniere. 2014. Seasonal changes in microbial community structure and activity imply winter production linked to summer hypoxia in a large lake system. FEMS Microbiology Ecology 87:475-485.
D’Souza, N.A.D., Y. Kawarasaki, J.D. Gantz, R.E. Lee, Jr., B.F.N. Beall, Y.M. Shtarkman, Z.A. Kocer, S.O. Rogers, H. Wildschutte, G.S. Bullerjahn, and R.M.L. McKay. 2013. Diatom assemblages promote ice formation in large lakes. ISME Journal 7: 1632-1640.
Small, G.E., G.S. Bullerjahn, R.W. Sterner, B.F.N. Beall, S. Brovold, J.C. Finlay, R.M.L. McKay, and M. Mukherjee. 2013. Rates and controls of nitrification in a large oligotrophic lake. Limnology and Oceanography, 58: 276-286.
Oyserman, B.O., LCDR W.C. Woityra, G.S. Bullerjahn, B.F.N. Beall, and R.M.L. McKay. 2012. Collecting winter data on U.S. Coast Guard icebreakers. Eos, Transactions, American Geophysical Union 93(10): 105-106.
Twiss, M.R., R.M.L. McKay, R.A. Bourbonniere, G.S. Bullerjahn, H.J. Carrick, R.E.H. Smith, J.G. Winter, N.A. D’Souza, P.C. Furey, A.R. Lashaway, M.A. Saxton, and S.W. Wilhelm. 2012. Diatoms abound in ice-covered Lake Erie: Investigation of offshore winter limnology in Lake Erie over the period 2007 to 2010. Journal of Great Lakes Research, 38: 18-30.