Aerosolization potential and activity in the limnic microalga Limnomonas gaiensis.

Aerosolization potential and activity in the limnic microalga Limnomonas gaiensis.
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Blind spots remain in deciphering the dispersion of microorganisms. Last century, Baas Beckning and Beijerinck, hypothesized that given a certain organismal size, "everything is everywhere, but, the environment selects"1, thus affecting organismal distribution over geographic and temporal scales. Uncovering organisms’ tolerance to environmental stressors would help understanding the species-specific chance of survival and possible mode of dispersal in nowadays and under climate-change scenarios.

 

Aquatic microorganisms, such as microalgae, can spread by water connectivity, human/animal movement, or air transportation2,3. Microalgal dispersal by water connectivity and water ballast has been widely investigated, but little is known on their dispersal mediated animal movements2,4,5 and air transportation3,6.

 

Green microalga belonging to the large polyphyletic genus Chlamydomonas are both present in aquatic- (over 581 species)7,8 and atmospheric habitats3. We recently described a Chlamydomonas-like species, Limnomonas gaiensis, present in freshwater lakes in Northern Europe9. Its peculiar morphology and motion permit a rapid recollection in natural samples9. The easiness of its barcoding and its distinct genetic signature can allow fast recognition in environmental samples9,10. Interestingly, the species shows signs of a recent expansion in unconnected water systems and of local adaptation10. Moreover, it presents key features for dispersal characterized by a potential to acclimate to a natural range of water temperatures, to a wide range of pH, and to short periods of desiccation10,11. The distance between the lakes in which L. gaiensis occurs diminished the likelihood for microalgal transportation by waterbirds and human activities. Thus, we wondered if the limnic L. gaiensis could be aerosolized, airborne dispersed, and spread between isolated lakes?

 

Microalgae can be aerosolized from aquatic sources mediated water surface abrasion and bubble bursting3. We simulated wave breaking, a technique that produces a broad size distribution of droplets that by rupturing can efficiently eject microalgae into the air12. Using this technique, our study shows that L. gaiensis can be aerosolized from water sources13, with an emission rate of several orders of magnitude higher than those previously recorded in the literature14,15.

 

From emission to deposition, multiple stressors can negatively impact microalgal survival. Microalgae have developed mechanisms that confer tolerance to atmospheric stressors16,17. Despite a high mortality rate, a small portion of emitted L. gaiensis could stay viable13. The species can tolerate short-term exposure to subzero temperatures down to -21°C and freezing events13. Also, the complex microalga-biont can produce volatile organic compounds (ethanol) and actively nucleate ice (mainly ≤-18°C)13.

 

The presence of active primary biological aerosol particles (PBAPs) can influence atmospheric processes18,19 such as aerosol and cloud optical properties, ice- and cloud condensation nuclei, and volatile organic compounds availability. The production of ethanol and ice nuclei associated with L. gaiensis strains occurred in relatively small amounts and at low temperature of activation compared to potent known PBAPs, respectively13. This suggests that L. gaiensis could potentially impact atmospheric processes, favoring their deposition and dispersal to new environments.

 

Limnomonas gaiensis could be widely dispersed in Northern European countries mediated air transportation. To decipher the species distribution and estimate its spreading direction and velocity, our study calls for phylogeographic investigations in freshwater lakes, in habitats where Chlamydomonas spp have been monitored.

 

References

1 de Wit, R & Bouvier, T. ‘Everything is everywhere, but, the environment selects’; what did Baas Becking and Beijerinck really say? Environmental Microbiology, 8, 4, 755–758 (2006). http://dx.doi.org/10.1111/j.1462-2920.2006.01017.x

2 Tesson, S.V.M. et al. Integrating microorganism and macroorganism dispersal: Modes, techniques and challenges with particular focus on co-dispersal. Ecoscience 22, 2–4, 109–124 (2016). https://dx.doi.org/10.1080/11956860.2016.1148458

3 Tesson, S.V.M. et al. Airborne microalgae: insights, opportunities and challenges. Appl. Environ. Microbiol. 82, 1978–1991 (2016). https://doi.org/10.1128/AEM.03333-15

4 Schlichting, H.E.Jr. The Role of Waterfowl in the Dispersal of Algae. Trans. Am. Micros. Soc. 79, 2, 160-166 (1960). https://doi.org/10.2307/3224082

5 Brochet, A.L., Guillemain, M., Fritz, H., Gauthier-Clerc, M. & Green, A.J. Plant dispersal by teal (Anas crecca) in the Camargue: duck guts are more important than their feet. Freshw. Biol. 55, 1262-1273 (2010). https://doi.org/10.1111/j.1365-2427.2009.02350.x

6 Wiśniewska, K., Lewandowska, A. & Śliwińska-Wilczewska, S. The importance of cyanobacteria and microalgae present in aerosols to human health and the environment–Review study. Environ. Int. 131, 104964 (2019). https://doi.org/10.1016/j.envint.2019.104964

7 Pröschold, T., Marin, B., Schlösser U.G. & Melkonian, M. Molecular Phylogeny and Taxonomic Revision of Chlamydomonas (Chlorophyta). I. Emendation of Chlamydomonas Ehrenberg and Chloromonas Gobi, and Description of Oogamochlamys gen. nov. and Lobochlamys gen. nov. Protist 152, 265-300 (2001). https://doi.org/10.1078/1434-4610-00068

8 Guiry, M.D. & Guiry, G.M. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway (2023). https://www.algaebase.org; searched on July 6, 2023.

9 Tesson, S.V.M. & Pröschold, T. Description of Limnomonas gen. nov., L. gaiensis sp. nov. and L. spitsbergensis sp. nov. (Chlamydomonadales, Chlorophyta). Diversity 14, 6, 481 (2022). https://doi.org/10.3390/d14060481

10 Sildever, S., Stewart, R.I.A. & Tesson, S.V.M. Factors contributing to the potential future expansion of Limnomonas gaiensis (Chlamydomonadales, Chlorophyta) in Northern European freshwater lakes. Eur. J. Phycol. (2023). https://doi.org/10.1080/09670262.2023.2274080

11 Tesson, S.V.M. Physiological responses to pH in the freshwater microalga Limnomonas gaiensis. J. Basic Microbiol. 1-13 (2023). https://doi.org/10.1002/jobm.202300107

12 Schlichting, H.E.Jr. Ejection of microalgae into the air via bursting bubbles. J Allergy Clin. Immunol. 53, 185–188 (1974). https://doi.org/10.1016/0091-6749(74)90006-2

13 Tesson, S.V.M, Barbato, M. & Rosati, B. Aerosolization flux, bio-products, and dispersal capacities in the freshwater microalga Limnomonas gaiensis (Chlorophyceae). Commun. Biol.  6, 809 (2023). https://doi.org/10.1038/s42003-023-05183-5

14 Brown Jr R.M., Larson D.A. & Bold H.C. Airborne algae: their abundance and heterogeneity. Science 143, 583–585 (1964). https://doi.org/10.1126/science.143.3606.583

15 Murby, A.L. & Haney, J.F. Field and laboratory methods to monitor lake aerosols for cyanobacteria and microcystins. Aerobiologia 32, 395–403 (2016). https://doi.org/10.1007/s10453-015-9409-z

16 Tesson, S.V.M. & Šantl-Temkiv, T. Ice nucleation activity and Aeolian dispersal success in airborne and aquatic microalgae. Front. Microbiol. 9, 2681 (2018). https://doi.org/10.3389/fmicb.2018.02681

17 Chiu, C.-S. et al. Mechanisms protect airborne green microalgae during long distance dispersal. Sci. Rep. 10, 13984 (2020). https://doi.org/10.1038/s41598-020-71004-y

18 Després, V. et al. Primary biological aerosol particles in the atmosphere: a review. Tellus B: Chem. Phys. Meteorol. 64, 1, 15598 (2012).  https://doi.org/10.3402/tellusb.v64i0.15598

19 Achyuthan, K.E. et al. Volatile Metabolites Emission by In Vivo Microalgae—An Overlooked Opportunity? Metabolites7, 39 (2017). https://doi.org/10.3390/metabo7030039

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Environmental Microbiology
Life Sciences > Biological Sciences > Microbiology > Environmental Microbiology
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