Extremophile Algae Threatened by Coastal Environmental Changes: Halophilic Microalgal Communities Are Resilient But Not Resistant — Oak Academic Publishing
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Extremophile Algae Threatened by Coastal Environmental Changes: Halophilic Microalgal Communities Are Resilient But Not Resistant
Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
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Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
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Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
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Chico Mendes Institute for Biodiversity Conservation, ICMBio, Brasília, Brazil
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Grants Office, Linköping University, Linköping, Sweden
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Department of Environmental Change, Linköping University, Linköping, Sweden
1 Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
2 Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
3 Institute of Biology, Federal University of Rio de Janeiro, Rio de Janeiro, Brazil
4 Chico Mendes Institute for Biodiversity Conservation, ICMBio, Brasília, Brazil
5 Grants Office, Linköping University, Linköping, Sweden
6 Department of Environmental Change, Linköping University, Linköping, Sweden
We examined the responses of extremophilic microalgal communities to environmental disturbance. Salt flat microbial mats are halophilic communities that thrive in extreme environments characterized by high salinity and frequent desiccation. However, they may be vulnerable to lower, mesophilic salinity levels resulting from accelerated hydrologic cycles and sea level rise caused by climate change. Therefore, we simulated these disturbance scenarios: one of a short-term extreme rainfall event and another of a long-term sea level rise. We measured the ecological and physiological effects of these scenarios by total and relative cell density, chlorophyll -a concentrations, diversity, equitability, richness, relative contribution per taxon, and taxonomic composition of the microalgal mats. We found that lower salinity levels significantly altered these parameters of extremophile microalgal communities and compromised their original functional traits. Short-term salinity stress, simulating extreme rainfall events, demonstrated the resilience of the microalgal mat community. After the disturbance, parameters returned to the original values, albeit with a minor taxonomic turnover. Long-term salinity stress, simulating sea-level rise, demonstrated the halophile community’s limited resistance. Community parameters quickly deviated from their original values and underwent significant changes. In both treatments, mesophilic salinities resulted in a loss of diversity and lower equitability. Maintaining high salinity levels emerged as pivotal for the stability of salt flat ecosystems. Restoration and management efforts should prioritize restoring field site salinities to previous baseline levels to facilitate the recovery of original functionality within these ecosystems. The lack of endemism in halophilic microalgal communities and the cosmopolitan distribution of our sampled taxa support the generality and applicability of our findings to salt flat microalgal communities worldwide. This study’s broader implications highlight the fragility and stenotolerance of apparently invulnerable extremophilic communities, underscoring the need for global conservation and management strategies to protect these delicate ecosystems in the face of a changing climate.
Pinckney, J.L. (2023) Benthic Microalgal Community Structure, Primary Productivity, and Fiddler Crab ( Leptuca pugilator ) Grazing in an Estuarine Salt Panne. Estuaries and Coasts , 46, 1316-1325. https://doi.org/10.1007/s12237-023-01208-8
Lin, W.J., Wu, J. and Lin, H.J. (2020) Contribution of Unvegetated Tidal Flats to Coastal Carbon Flux. Global Change Biology , 26, 3443-3454. https://doi.org/10.1111/gcb.15107
Shadrin, N.V. and Anufriieva, E.V. (2020) Structure and Trophic Relations in Hypersaline Environments. Biology Bulletin Reviews , 10, 48-56. https://doi.org/10.1134/s2079086420010065
Ferreira, A.C., Freire, F.A.M., Rodrigues, J.V.M. and Bezerra, L.E.A. (2022) Mangrove Recovery in Semiarid Coast Shows Increase of Ecological Processes from Biotic and Abiotic Drivers in Response to Hydrological Restoration. Wetlands , 42, Article No. 80. https://doi.org/10.1007/s13157-022-01603-0
Oren, A. (2015) Halophilic Microbial Communities and Their Environments. Current Opinion in Biotechnology , 33, 119-124. https://doi.org/10.1016/j.copbio.2015.02.005
Vadeboncoeur, Y., Lodge, D.M. and Carpenter, S.R. (2001) Whole-Lake Fertilization Effects on Distribution of Primary Production between Benthic and Pelagic Habitats. Ecology , 82, 1065-1077.
Chen, Z.L. and Lee, S.Y. (2022) Tidal Flats as a Significant Carbon Reservoir in Global Coastal Ecosystems. Frontiers in Marine Science , 9, Article 900896. https://doi.org/10.3389/fmars.2022.900896
Costa, C.S.B. and Herrera, O.B. (2016) Halophytic Life in Brazilian Salt Flats: Biodiversity, Uses and Threats. In: Khan, M.A., Boër, B., Ȫzturk, M., Clüsener-Godt, M., Gul, B. and Breckle, S.W., Sabkha Ecosystems : Volume V : The Americas , Springer International Publishing, 11-27.
Banda, J.F., Lu, Y., Hao, C., Pei, L., Du, Z., Zhang, Y., et al . (2019) The Effects of Salinity and pH on Microbial Community Diversity and Distribution Pattern in the Brines of Soda Lakes in Badain Jaran Desert, China. Geomicrobiology Journal , 37, 1-12. https://doi.org/10.1080/01490451.2019.1654568
Uritskiy, G., Getsin, S., Munn, A., Gomez-Silva, B., Davila, A., Glass, B., et al . (2019) Halophilic Microbial Community Compositional Shift after a Rare Rainfall in the Atacama Desert. The ISME Journal , 13, 2737-2749. https://doi.org/10.1038/s41396-019-0468-y
FitzGerald, D.M. and Hughes, Z. (2019) Marsh Processes and Their Response to Climate Change and Sea-Level Rise. Annual Review of Earth and Planetary Sciences , 47, 481-517. https://doi.org/10.1146/annurev-earth-082517-010255
Van Meerbeek, K., Jucker, T. and Svenning, J. (2021) Unifying the Concepts of Stability and Resilience in Ecology. Journal of Ecology , 109, 3114-3132. https://doi.org/10.1111/1365-2745.13651
Serejo, M.L., Franco Morgado, M., García, D., González-Sánchez, A., Méndez-Acosta, H.O. and Toledo-Cervantes, A. (2020) Environmental Resilience by Microalgae. In: Microalgae Cultivation for Biofuels Production , Elsevier, 293-315. https://doi.org/10.1016/b978-0-12-817536-1.00019-9
Cheng, L., Trenberth, K.E., Gruber, N., Abraham, J.P., Fasullo, J.T., Li, G., et al . (2020) Improved Estimates of Changes in Upper Ocean Salinity and the Hydrological Cycle. Journal of Climate , 33, 10357-10381. https://doi.org/10.1175/jcli-d-20-0366.1
Benestad, R.E., Lussana, C., Lutz, J., Dobler, A., Landgren, O., Haugen, J.E., et al . (2022) Global Hydro-Climatological Indicators and Changes in the Global Hydrological Cycle and Rainfall Patterns. PLOS Climate , 1, e0000029. https://doi.org/10.1371/journal.pclm.0000029
Fowler, H.J., Ali, H., Allan, R.P., Ban, N., Barbero, R., Berg, P., et al . (2021) Towards Advancing Scientific Knowledge of Climate Change Impacts on Short-Duration Rainfall Extremes. Philosophical Transactions of the Royal Society A : Mathematical, Physical and Engineering Sciences , 379, Article 20190542. https://doi.org/10.1098/rsta.2019.0542
Martel, J.L., Brissette, F.P., Lucas-Picher, P., Troin, M. and Arsenault, R. (2021) Climate Change and Rainfall Intensity-Duration-Frequency Curves: Overview of Science and Guidelines for Adaptation. Journal of Hydrologic Engineering , 26, Article 03121001. https://doi.org/10.1061/(asce)he.1943-5584.0002122
He, Q. and Silliman, B.R. (2019) Climate Change, Human Impacts, and Coastal Ecosystems in the Anthropocene. Current Biology , 29, R1021-R1035. https://doi.org/10.1016/j.cub.2019.08.042
Saintilan, N., Khan, N.S., Ashe, E., Kelleway, J.J., Rogers, K., Woodroffe, C.D., et al . (2020) Thresholds of Mangrove Survival under Rapid Sea Level Rise. Science , 368, 1118-1121. https://doi.org/10.1126/science.aba2656
Nicholls, R.J., Lincke, D., Hinkel, J., Brown, S., Vafeidis, A.T., Meyssignac, B., et al . (2021) A Global Analysis of Subsidence, Relative Sea-Level Change and Coastal Flood Exposure. Nature Climate Change , 11, 338-342. https://doi.org/10.1038/s41558-021-00993-z
Abomohra, A.E.F., El-Naggar, A.H., Alaswad, S.O., Elsayed, M., Li, M. and Li, W. (2020) Enhancement of Biodiesel Yield from a Halophilic Green Microalga Isolated under Extreme Hypersaline Conditions through Stepwise Salinity Adaptation Strategy. Bioresource Technology , 310, Article 123462. https://www.sciencedirect.com/science/article/pii/S0960852420307343?casa_token=zBTzhbI4sO0AAAAA:zQs32xsTCA03SUJ6-R_CfCwKyJTjYh6V5k7wDPOmAIRW7tsVMVULxrQtfKH1qSLas3TOdEisju4q
Barut, D., Enuh, B.M., Derkuş, B., Güler, Ü., Salih, B. and Aytar Çelik, P. (2023) The Relationship between Bacterial Outer Membrane Vesicles and Halophilic Adaptation. Molecular Omics , 19, 174-181. https://doi.org/10.1039/d2mo00259k
Yoo, Y., Lee, H., Lee, J., Khim, J.S. and Kim, J. (2023) Insights into Saline Adaptation Strategies through a Novel Halophilic Bacterium Isolated from Solar Saltern of Yellow Sea. Frontiers in Marine Science , 10, Article 1229444. https://doi.org/10.3389/fmars.2023.1229444
INPE (2023) Centro de Previsão de Tempo e Estudos Climáticos. http://clima.cptec.inpe.br/
Chaves, F., Gomes, J., Soares, M., Estrada, G., Almeida, P.M. and Cavalcanti, V. (2013) Contribution to Knowledge and Conservation of the Guaratiba Coastal Plain—Sepetiba bay, Rio de Janeiro-Brazil. Journal of Integrated Coastal Zone Management , 13, 123-136.
Panja, A.K., Vasavdutta, S., Choudhary, M., Thiyagarajan, I., Shinde, A.H., Ray, S., et al . (2023) Interaction of Physico-Chemical Parameters with Shannon-Weaver Diversity Index Based on Phytoplankton Diversity in Coastal Water of Diu, India. Marine Pollutio n Bulletin , 190, Article 114839. https://doi.org/10.1016/j.marpolbul.2023.114839
Tarafdar, L., Kim, J.Y., Srichandan, S., Mohapatra, M., Muduli, P.R., Kumar, A., et al . (2021) Responses of Phytoplankton Community Structure and Association to Variability in Environmental Drivers in a Tropical Coastal Lagoon. Science of the Total Environment , 783, Article 146873. https://doi.org/10.1016/j.scitotenv.2021.146873
Siedlewicz, G., Żak, A., Sharma, L., Kosakowska, A. and Pazdro, K. (2020) Effects of Oxytetracycline on Growth and Chlorophyll a Fluorescence in Green Algae ( Chlorella vulgaris ), Diatom ( Phaeodactylum tricornutum ) and Cyanobacteria ( Microcystis aeruginosa and Nodularia spumigena ). Oceanologia , 62, 214-225. https://doi.org/10.1016/j.oceano.2019.12.002
Jeffrey, S.W. and Humphrey, G.F. (1975) New Spectrophotometric Equations for Determining Chlorophylls A, B, C1 and C2 in Higher Plants, Algae and Natural Phytoplankton. Biochemie und Physiologie der Pflanzen , 167, 191-194. https://doi.org/10.1016/s0015-3796(17)30778-3
R Core Team (2023) R Development Core Team R: A Language and Environment for Statistical Computing 2023. R Core Team.
Bento, L., Masuda, L.S.M., Peixoto, R.B. and Enrich-Prast, A. (2017) Regulation in the Metabolism and Community Structure of a Tropical Salt Flat after Rainfall. Journal of Coastal Research , 332, 304-308. https://doi.org/10.2112/jcoastres-d-15-00179.1
Creed, J.C., Vieira, V.M.N.C.S., Norton, T.A. and Caetano, D. (2019) A Meta-Analysis Shows That Seaweeds Surpass Plants, Setting Life-on-Earth’s Limit for Biomass Packing. BMC Ecology , 19, Article No. 6. https://doi.org/10.1186/s12898-019-0218-z
Borics, G., Abonyi, A., Salmaso, N. and Ptacnik, R. (2021) Freshwater Phytoplankton Diversity: Models, Drivers and Implications for Ecosystem Properties. Hydrobiologia , 848, 53-75. https://doi.org/10.1007/s10750-020-04332-9
Shu, W.S. and Huang, L.N. (2022) Microbial Diversity in Extreme Environments. Nature Reviews Microbiology , 20, 219-235. https://doi.org/10.1038/s41579-021-00648-y
Couso, L.L., Soler‐Bistué, A., Aptekmann, A.A. and Sánchez, I.E. (2023) Ecology Theory Disentangles Microbial Dichotomies. Environmental Microbiology , 25, 3052-3063. https://doi.org/10.1111/1462-2920.16495
Bartha, E. (2022) Investigating Extremotolerant Microbes in Non-Extreme Environments and Altering the Salinity Growth Limits of Halophiles. Ph.D. Thesis, University of Essex. https://repository.essex.ac.uk/33275/
Zhou, X., Chen, X., Qi, X., Zeng, Y., Guo, X., Zhuang, G., et al . (2023) Soil Bacterial Communities Associated with Multi-Nutrient Cycling under Long-Term Warming in the Alpine Meadow. Frontiers in Microbiology , 14, Article 1136187. https://doi.org/10.3389/fmicb.2023.1136187
Clark, D.R., Mathieu, M., Mourot, L., Dufossé, L., Underwood, G.J.C., Dumbrell, A.J., et al . (2017) Biogeography at the Limits of Life: Do Extremophilic Microbial Communities Show Biogeographical Regionalization? Global Ecology and Biogeography , 26, 1435-1446. https://doi.org/10.1111/geb.12670