Articles | Volume 20, issue 13
https://doi.org/10.5194/bg-20-2805-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/bg-20-2805-2023
© Author(s) 2023. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Research article
| 
14 Jul 2023
Research article |
| 14 Jul 2023
| 14 Jul 2023
Lichen species across Alaska produce highly active and stable ice nucleators
Rosemary J. Eufemio
Department of Chemistry and Biochemistry, Boise State University,
Boise, ID 83725, USA
Biomolecular Sciences Graduate Programs, Boise State University,
Boise, ID 83725, USA
Ingrid de Almeida Ribeiro
Department of Chemistry, The University of Utah, Salt Lake City, UT 84112, USA
Todd L. Sformo
Institute of Arctic Biology, University of Alaska Fairbanks,
Fairbanks, AK 99775, USA
Gary A. Laursen
High Latitude Mycological Research Institute, University of Montana,
Missoula, MT 59801, USA
Valeria Molinero
Department of Chemistry, The University of Utah, Salt Lake City, UT 84112, USA
Janine Fröhlich-Nowoisky
Max Planck Institute for Chemistry, 55128 Mainz, Germany
Mischa Bonn
Max Planck Institute for Polymer Research, 55128 Mainz, Germany
Konrad Meister
CORRESPONDING AUTHOR
Department of Chemistry and Biochemistry, Boise State University,
Boise, ID 83725, USA
Max Planck Institute for Polymer Research, 55128 Mainz, Germany
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Cited articles
Budke, C. and Koop, T.: BINARY: an optical freezing array for assessing temperature and time dependence of heterogeneous ice nucleation, Atmos. Meas. Tech., 8, 689–703, https://doi.org/10.5194/amt-8-689-2015, 2015.
Creamean, J. M., Ceniceros, J. E., Newman, L., Pace, A. D., Hill, T. C. J., DeMott, P. J., and Rhodes, M. E.: Evaluating the potential for Haloarchaea to serve as ice nucleating particles, Biogeosciences, 18, 3751–3762, https://doi.org/10.5194/bg-18-3751-2021, 2021.
de Almeida Ribeiro, I., Meister, K., and Molinero, V.: HUB: A method to
model and extract the distribution of ice nucleation temperatures from
drop-freezing experiments, ChemRxiv, Cambridge, https://doi.org/10.26434/chemrxiv-2022-ddzv8, 2022.
Dreischmeier, K., Budke, C., Wiehemeier, L., Kottke, T., and Koop, T.:
Boreal pollen contain ice-nucleating as well as ice-binding “antifreeze”
polysaccharides, Sci. Rep., 7, 1–13,
https://doi.org/10.1038/srep41890, 2017.
Fröhlich-Nowoisky, J., Pickersgill, D. A., Despré, V. R., and
Pöschl, U.: High diversity of fungi in air particulate matter, P. Natl. Acad. Sci. USA,
106, 12814–12819, 2009.
Fröhlich-Nowoisky, J., Burrows, S. M., Xie, Z., Engling, G., Solomon, P. A., Fraser, M. P., Mayol-Bracero, O. L., Artaxo, P., Begerow, D., Conrad, R., Andreae, M. O., Després, V. R., and Pöschl, U.: Biogeography in the air: fungal diversity over land and oceans, Biogeosciences, 9, 1125–1136, https://doi.org/10.5194/bg-9-1125-2012, 2012.
Fröhlich-Nowoisky, J., Hill, T. C. J., Pummer, B. G., Yordanova, P., Franc, G. D., and Pöschl, U.: Ice nucleation activity in the widespread soil fungus Mortierella alpina, Biogeosciences, 12, 1057–1071, https://doi.org/10.5194/bg-12-1057-2015, 2015.
Govindarajan, A. G. and Lindow, S. E.: Size of bacterial ice-nucleation
sites measured in situ by radiation inactivation analysis, P. Natl. Acad. Sci. USA, 85,
1334–1338, https://doi.org/10.1073/PNAS.85.5.1334, 1988.
Henderson-Begg, S. K., Hill, T., Thyrhaug, R., Khan, M., and Moffett, B. F.:
Terrestrial and airborne non-bacterial ice nuclei,
Atmos. Sci. Lett., 10, 215–219, https://doi.org/10.1002/ASL.241, 2009.
Honegger, R.: Water relations in lichens, in: Fungi in the Environment,
edited by: Gadd, G. M., Watkinson, S. C., Dyer, P, Cambridge University
Press, Cambridge, 185–200, https://doi.org/10.1017/CBO9780511541797.010,
2007.
Kieft, T. L. and Ahmadjian, V.: Biological Ice Nucleation Activity in Lichen
Mycobionts and Photobionts, The Lichenologist, 21, 355–362,
https://doi.org/10.1017/S0024282989000599, 1989.
Kieft, T. L. and Lindow, S.: Ice Nucleation Activity in Lichens, Appl.
Environ. Microbiol., 54, 1678–1681, 1988.
Kieft, T. L. and Ruscetti, T.: Characterization of Biological Ice Nuclei
from a Lichen, J. Bacteriol., 172, 3519–3523, 1990.
Koop, T., Luo, B., Tsias, A., and Peter, T.: Water activity as the
determinant for homogeneous ice nucleation in aqueous solutions, Nature,
406, 611–614, https://doi.org/10.1038/35020537, 2000.
Kozloff, L. M., Schofield, M. A., and Lute, M.: Ice nucleating activity of
Pseudomonas syringae and Erwinia herbicola, J. Bacteriol., 153, 222–231,
https://doi.org/10.1128/JB.153.1.222-231.1983, 1983.
Kunert, A. T., Lamneck, M., Helleis, F., Pöschl, U., Pöhlker, M. L., and Fröhlich-Nowoisky, J.: Twin-plate Ice Nucleation Assay (TINA) with infrared detection for high-throughput droplet freezing experiments with biological ice nuclei in laboratory and field samples, Atmos. Meas. Tech., 11, 6327–6337, https://doi.org/10.5194/amt-11-6327-2018, 2018.
Kunert, A. T., Pöhlker, M. L., Tang, K., Krevert, C. S., Wieder, C., Speth, K. R., Hanson, L. E., Morris, C. E., Schmale III, D. G., Pöschl, U., and Fröhlich-Nowoisky, J.: Macromolecular fungal ice nuclei in Fusarium: effects of physical and chemical processing, Biogeosciences, 16, 4647–4659, https://doi.org/10.5194/bg-16-4647-2019, 2019.
Lukas, M., Schwidetzky, R., Kunert, A. T., Pöschl, U.,
Fröhlich-Nowoisky, J., Bonn, M., and Meister, K.: Electrostatic
Interactions Control the Functionality of Bacterial Ice Nucleators, J. Am.
Chem. Soc., 142, 6842–6846, https://doi.org/10.1021/jacs.9b13069, 2020.
Lundheim, R.: Physiological and ecological significance of biological ice
nucleators, Philos. Trans. R. Soc. Lond. Series B, Biol. Sci., 357,
937–943, https://doi.org/10.1098/rstb.2002.1082, 2002.
Maki, L. R. and Willoughby, K. J.: Bacteria as biogenic sources of freezing
nuclei, J. Appl. Meteorol. Climatol., 17, 1049–1053, 1978.
Maki, L. R., Galyan, E. L., Chang-Chien, M. M., and Caldwell, D. R.: Ice
Nucleation Induced by Pseudomonas syringae, Appl. Microbiol., 28, 456–459,
https://doi.org/10.1128/AM.28.3.456-459.1974, 1974.
Moffett, B. F., Getti, G., Henderson-Begg, S. K., and Hill, T. C. J.:
Ubiquity of ice nucleation in lichen – possible atmospheric implications,
Lindbergia, 38, 39–43, https://doi.org/10.25227/linbg.01070, 2015.
Murray, B. J., O'sullivan, D., Atkinson, J. D., and Webb, M. E.: Ice
nucleation by particles immersed in supercooled cloud droplets, Chem. Soc.
Rev., 41, 6519–6554, https://doi.org/10.1039/c2cs35200a, 2012.
Pojar, J. and MacKinnon, A. (Eds.): Plants of the Pacific Northwest Coast:
Washington, Oregon, British Columbia, & Alaska, Lone Pine Publishing,
Canada, 484–504, ISBN 1-55105-040-4, 1994.
Polen, M., Lawlis, E., and Sullivan, R. C.: The unstable ice nucleation
properties of Snomax® bacterial particles, J. Geophys. Res.
Atmos., 121, 11666–11678, https://doi.org/10.1002/2016JD025251, 2016.
Pouleur, S., Richard, C., Martin, J., and Antoun, H.: Ice Nucleation
Activity in Fusarium acuminatum and Fusarium avenaceum, Appl. Environ.
Microbiol., 58, 2960–2964, https://doi.org/10.1128/AEM.58.9.2960-2964.1992,
1992.
Pummer, B. G., Bauer, H., Bernardi, J., Bleicher, S., and Grothe, H.: Suspendable macromolecules are responsible for ice nucleation activity of birch and conifer pollen, Atmos. Chem. Phys., 12, 2541–2550, https://doi.org/10.5194/acp-12-2541-2012, 2012.
Qiu, Y., Hudait, A., and Molinero, V.: How size and aggregation of
ice-binding proteins control their ice nucleation efficiency, J. Am. Chem.
Soc., 141, 7439–7452, 2019.
Schwidetzky, R., Sudera, P., Backes, A. T., Pöschl, U., Bonn, M.,
Fröhlich-Nowoisky, J., and Meister, K.: Membranes Are Decisive for
Maximum Freezing Efficiency of Bacterial Ice Nucleators, J. Phys. Chem.
Lett., 12, 10783–10787, https://doi.org/10.1021/acs.jpclett.1c03118, 2021a.
Schwidetzky, R., Lukas, M., YazdanYar, A., Kunert, A. T., Pöschl, U.,
Domke, K. F., Fröhlich-Nowoisky, J., Bonn, M., Koop, T., Nagata, Y., and
Meister, K.: Specific Ion–Protein Interactions Influence Bacterial Ice
Nucleation, Chem.-A Eur. J., 27, 7402–7407,
https://doi.org/10.1002/CHEM.202004630, 2021b.
Simpson, J. J., Stuart, M. C., and Daly, C.: A discriminant analysis model
of Alaskan biomes based on spatial climatic and environmental data, Arctic,
60, 341–369, 2007.
Turner, M. A., Arellano, F., and Kozloff, L. M.: Three separate classes of
bacterial ice nucleation structures, J. Bacteriol., 172, 2521–2526,
https://doi.org/10.1128/JB.172.5.2521-2526.1990, 1990.
Vali, G.: Quantitative evaluation of experimental results and the
heterogeneous freezing nucleation of supercooled liquids, J. Atmos. Sci.,
28, 402–409, 1971.
Wilson, P. W., Heneghan, A. F., and Haymet, A. D. J.: Ice nucleation in
nature: supercooling point (SCP) measurements and the role of heterogeneous
nucleation, Cryobiology, 46, 88–98,
https://doi.org/10.1016/S0011-2240(02)00182-7, 2003.
Womack, A. M., Artaxo, P. E., Ishida, F. Y., Mueller, R. C., Saleska, S. R., Wiedemann, K. T., Bohannan, B. J. M., and Green, J. L.: Characterization of active and total fungal communities in the atmosphere over the Amazon rainforest, Biogeosciences, 12, 6337–6349, https://doi.org/10.5194/bg-12-6337-2015, 2015.
Yang, S., Rojas, M., Coleman, J. J., and Vinatzer, B. A.: Identification of
Candidate Ice Nucleation Activity (INA) Genes in Fusarium avenaceum by
Combining Phenotypic Characterization with Comparative Genomics and
Transcriptomics, Journal of Fungi, 8, 958,
https://doi.org/10.3390/JOF8090958/S1, 2022.
Zachariassen, K. E. and Kristiansen, E.: Ice Nucleation and Antinucleation
in Nature, Cryobiology, 41, 257–279,
https://doi.org/10.1006/CRYO.2000.2289, 2000.
Short summary
Lichens, the dominant vegetation in the Arctic, contain ice nucleators (INs) that enable freezing close to 0°C. Yet the abundance, diversity, and function of lichen INs is unknown. Our screening of lichens across Alaska reveal that most species have potent INs. We find that lichens contain two IN populations which retain activity under environmentally relevant conditions. The ubiquity and stability of lichen INs suggest that they may have considerable impacts on local atmospheric patterns.
Lichens, the dominant vegetation in the Arctic, contain ice nucleators (INs) that enable...
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