Homogenization of lake cyanobacterial communities over a century of climate change and eutrophication

Abstract

Human impacts on biodiversity are well recognized, but uncertainties remain regarding patterns of diversity change at different spatial and temporal scales. Changes in microbial assemblages are, in particular, not well understood, partly due to the lack of community composition data over relevant scales of space and time. Here, we investigate biodiversity patterns in cyanobacterial assemblages over one century of eutrophication and climate change by sequencing DNA preserved in the sediments of ten European peri-Alpine lakes. We found species losses and gains at the lake scale, while species richness increased at the regional scale over approximately the past 100 years. Our data show a clear signal for beta diversity loss, with the composition and phylogenetic structure of assemblages becoming more similar across sites in the most recent decades, as have the general environmental conditions in and around the lakes. We attribute patterns of change in community composition to raised temperatures affecting the strength of the thermal stratification and, as a consequence, nutrient fluctuations, which favoured cyanobacterial taxa able to regulate buoyancy. Our results reinforce previous reports of human-induced homogenization of natural communities and reveal how potentially toxic and bloom-forming cyanobacteria have widened their geographic distribution in the European temperate region.

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Fig. 1: History of environmental conditions in the ten peri-Alpine lakes.
Fig. 2: Changes in cyanobacterial OTU richness and phylogenetic structure.
Fig. 3: Proportion of rare and common OTUs across all lakes.
Fig. 4: OTU richness change within cyanobacterial orders.
Fig. 5: Prevalence of OTUs in all lakes between the 1900s and 2015.

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Acknowledgements

The high-throughput sequencing data were produced at Fasteris (Geneva). We thank J.-C. Walser (Genetic Diversity Centre, ETH Zürich) for bioinformatics support and B. Müller for helping with the lake chemical data acquisition. We thank M. Thali, A. Lück, A. Zwyssig, C. Chardon, A. Lami, S. Gerli, H. Penson and C. Ouellet-Plamondon for technical assistance, as well as M. Lavrieux for help with the sediment dating. We are grateful to I. Gregory-Eaves, H. Hartikainen, R. Ptacnik, K. Räsänen, C. Tellenbach and M. K. Thomas for intellectual feedback and fruitful discussions. Coring, dating and DNA extractions for lakes Annecy and Geneva were performed in the context of the 'REPLAY' programme funded by the Structural Ecosphere Continent and Coastal Initiative at the Institut National des Sciences de l'Univers and the Iper Retro programme funded by the Agence Nationale de la Recherche VULNS-005 (France). The physical and chemical data were produced by Amt für Abfall, Wasser, Energie und Luft (Canton Zurich) for Greifensee, Wasserversorgung Zürich for Lake Zurich, Lake Constance Water Supply for Lake Constance, Abteilung für Umwelt Kanton Aargau (A. Stöckli) for Hallwilersee, Eawag/Kanton Luzern for Baldeggersee, the Swiss Federal Office for the Environment and F. Lepori at the Istituto Scienze della Terra, ITS SUPSI, Lugano for Lake Lugano, M. Manca (Consiglio Nazionale delle Ricerche, Institute of Ecosystem Study, Italy) for Lake Maggiore, the Observatory of the Alpine Lakes, Commission Internationale pour la Protection des Eaux du Léman (CIPEL), Syndicat Mixte du Lac d'Annecy (SILA) and Système d'Information de l'Observatoire des Lacs Alpins (OLA-IS) developed by Eco-Informatics, Observatoire Recherche en Environnement (ORE INRA) for the lakes Annecy and Geneva and G. Tartari (Istituto di Ricerca sulle Acque, Consiglio Nazionale delle Ricerche, Brugherio, Italy) for Lake Pusiano. This work was supported by the Swiss Enlargement Contribution, project IZERZ0 – 142165, 'CyanoArchive' to P.S., in the framework of the Romanian–Swiss Research Programme.

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M.-E.M., P.S. and F.P. designed the study. I.D. and N.D. contributed the materials and analysis tools and samples. M.-E.M. and I.D. collected the data. All analyses were carried out by M.-E.M. and D.B. M.-E.M. and F.P. wrote the manuscript, which was revised and edited by all authors.

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Correspondence to Marie-Eve Monchamp or Francesco Pomati.

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Supplementary Figures 1–4

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Supplementary Table 1

Overview of lake characteristics. List of lakes geographical location, main morphological characteristics, and current trophic status

Supplementary Table 2

Overview of lake chemical data used in this study. The table includes the source of phosphorus and nitrogen data, and the duration of the nutrient time series used in this study

Supplementary Table 3

List of all samples used in this study. The table includes the sample ID, the PCR primer sequences and the tag sequences used in the sequencing library preparation

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Monchamp, M., Spaak, P., Domaizon, I. et al. Homogenization of lake cyanobacterial communities over a century of climate change and eutrophication. Nat Ecol Evol 2, 317–324 (2018). https://doi.org/10.1038/s41559-017-0407-0

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