The Enigma Of Biological Ice Nucleators
Guest Post by Cindy E. Morris1,2 and David C. Sands2
1INRA, Plant Pathology research unit, F-84140 Montfavet, France, cindy.morris@avignon.inra.fr
2Dept. Plant Sciences and Plant Pathology, 119 Plant Biosciences Bldg., Montana State University, Bozeman, MT 59717-3150, USA, davidsands41@yahoo.com
In the mid 1970’s several research groups discovered independently that the plant pathogenic bacterium Pseudomonas syringae was a very active ice nucleator (2, 5, 10). Although other organisms have since been discovered to have ice nucleation activity, P. syringae and related bacteria still hold the title of producing ice nuclei active at the warmest temperatures observed in nature (up to -1° to -2°C). As a plant epiphyte (surface colonizer) and pathogen, P. syringae inhabits principally the aerial parts of plants. Hence, like other organisms that live on aerial plant surfaces these bacteria are readily disseminated by the wind. So it is not surprising that this bacterium is transported up into clouds, as has been demonstrated by several different research teams (1, 9). In the daily routine of plant pathologists, who care a great deal about modes of disease transmission, this is just another example of effective aerial dissemination accomplished by microbial cells with just the right aerodynamic properties to be trapped and propelled by air masses. Disease epidemiology and disease prediction are the natural confluence of biology with meteorology.
For most organisms that produce ice nuclei, there is some apparent environmental impact and some selective advantage of this capacity. Most organisms that produce ice nuclei, such as plants and insects, live in habitats where they regularly encounter sub zero temperatures. In most cases, by inducing ice formation, these organisms avoid the damage that would be caused to their cells by ice that would otherwise form at much colder temperatures had they not induced the ice. For bacteria, there are several hypotheses about the forces of nature that could be selecting for ice nucleation activity. One hypothesis is that by inducing frost damage to the plants with which it lives, P. syringae gains access to nutrients (cellular contents of leaves) when the tissue is damaged. A second hypothesis is that ice nucleation activity aids the bacterium in its dissemination by causing ice formation (and subsequently raindrops) in clouds thereby facilitating its escape from the atmosphere and its return to terrestrial habitats (7). This dissemination hypothesis extends far beyond the realm of plant pathology because it suggests that micro-organisms could have some role in the physical processes that lead to precipitation (6). This question has intrigued both microbiologists and atmosphere physicists alike. It would be very honest to state that the intrigue has been, over the past decades, counterbalanced by a sense of unease in both camps because of unfamiliarity with the evidence criteria expected in each field for hypothesis verification.
In 2006 with funding from the European Science Foundation, we organized an exploratory workshop in Avignon France entitled “Microbiological Meteorology”. This workshop brought together atmosphere physicists and chemists with microbiologists, agronomists and modelers in an effort to build bridges necessary to explore the potential interaction of micro-organisms with phenomena implicated in weather. The final report from the workshop is at: http://www.esf.org/index.php?eID=tx_nawsecuredl&u=0&file=fileadmin/be_user/ew_docs/05-038_Report.pdf&t=1264027975&hash=aacead61000754902573c5ac31bc17b5. This workshop was followed by a session on “Biological Ice Nucleators in the Atmosphere” at the 2007 annual meeting of the Int. Union of Geophysics and Geodesy. In 2009 biologists were included for the first time at the International Conference on Nucleation and Atmospheric Aerosols. These initial contacts have resulted in some exciting publications (3, 4, 8), the emergence of new interdisciplinary projects that address questions related to the potential role of biological ice nucleators in precipitation, in lively exchanges on our mailing list (contact C.E. Morris if you want your name added), the accumulation of resource information on our internet discussion forum (www.bio-ice.forumotion.com) and overwhelming interest by the media as exemplified by a recent BBC broadcast (http://www.bbc.co.uk/programmes/p004lf1f#broadcasts). They have also re-enforced our impression that the question about the role of biological ice nucleators in precipitation is worth pursuing.
Yet, on the other hand we are confronted by interrogations about the real capacity of these biological particles to have significant impacts on the atmosphere given their low numbers (probably less than 10’s per m3 of air) relative to inert ice nucleators that are thousands of times more abundant. It is not clear if ice nucleation that occurs at warm temperatures could lead to the formation of ice that could grow enough to fall out as precipitation or that could propagate through the multiplicative Hallett-Mossop process. We are still in the stage of birthing and nurturing some risky research and of sticking our necks out to potentially be chopped in the long run.
The stakes are high. Biological ice nucleators such as P. syringae are the products of agriculture in that they can be very abundant on crops. Hence, one of the outcomes of this research could be a fuller understanding of how the plants in landscapes impact weather. The research by Dr. Pielke and his colleagues and contemporaries clearly illustrate that plants affect rainfall. Part of this impact might be assured by the biological ice nucleators that are part and parcel of the plants. And, as the micro-flora of plants is determined in part by the genetic background of plants and their physiological state, this means that there could be coordinated efforts in plant breeding, agronomy and phytobacteriology for enhancing plant microflora to intensify their contribution to rainfall. We wonder how to best tease out of the complex biosphere system the answers to questions about the raison d’être of biological ice nucleation and its environmental impacts and the extent to which this potential effect could be tweaked to offset the impacts of climate change. We look forward to debate.
References
1. Amato, P., M. Parazols, M. Sancelme, P. Laj, G. Mailhot, and A.-M. Delort. 2007. Microorganisms isolated from the water phase of tropospheric clouds at the Puy de Dôme: major groups and growth abilities at low temperatures. FEMS Microbiol. Ecol. 59:242-254.
2. Arny, D. C., S. E. Lindow, and C. D. Upper. 1976. Frost sensitivity of Zea mays increased by application of Pseudomonas syringae. Nature 262:282-284.
3. Christner, B. C., C. E. Morris, C. M. Foreman, R. Cai, and D. C. Sands. 2008. Ubiquity of biological ice nucleators in snowfall. Science 319:1214.
4. Christner, B. C., C. Rongman, C. E. Morris, K. S. McCarter, C. M. Foreman, M. L. Skidmore, S. N. Montross, and D. C. Sands. 2008. Geographic location, season, and precipitation chemistry influence on the abundance and activity of biological ice nucleators in rain and snow. Proc. Nat. Acad. Sci. 105:18854–18859.
5. Maki, L. R., E. L. Gaylan, M. M. Chang-Chien, and D. R. Caldwell. 1974. Ice nucleation induced by Pseudomonas syringae. Appl. Microbiol. 28:456-459.
6. Morris, C. E., D. Georgakapolous, and D. C. Sands. 2004. Ice nucleation active bacteria and their potential role in precipitation. J. Phys. IV, France 121:87-103.
7. Morris, C. E., D. C. Sands, B. A. Vinatzer, C. Glaux, C. Guilbaud, A. Buffière, S. Yan, H. Dominguez, and B. M. Thompson. 2008. The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME Journal 2:321-334.
8. Pratt, K. A., P. J. DeMott, J. R. French, Z. Wang, D. L. Westphal, A. J. Heymsfield, C. H. Twohy, A. J. Prenni, and K. A. Prather. 2009. In situ detection of biological particles in cloud ice-crystals. Nature Geosci.
9. Sands, D. C., V. E. Langhans, A. L. Scharen, and G. de Smet. 1982. The association between bacteria and rain and possible resultant meteorological implications. J. Hungarian Meteorol. Serv. 86:148-152.
10. Upper, C. D., and G. Vali. 1995. The discovery of bacterial ice nucleation and its role in the injury of plants by frost., p. 29-41. In R. E. Lee, Jr., G. J. Warren, and L. V. Gusta (ed.), Biological Ice Nucleation and its Applications. APS Press, St. Paul.
