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Sedimentary DNA Reveals Centuries of Hidden Diversity in Lake Cyanobacterial Communities

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Research Collection Doctoral Thesis Sedimentary DNA reveals centuries of hidden diversity in lake cyanobacterial communities Author(s): Monchamp, Marie-Eve Publication Date: 2017 Permanent Link: https://doi.org/10.3929/ethz-b-000166606 Rights / License: In Copyright - Non-Commercial Use Permitted This page was generated automatically upon download from the ETH Zurich Research Collection. For more information please consult the Terms of use. ETH Library DISS. ETH NO. 24227 Sedimentary DNA reveals centuries of hidden diversity in lake cyanobacterial communities A thesis submitted to attain the degree of DOCTOR OF SCIENCES of ETH ZURICH (Dr. sc. ETH Zurich) presented by MARIE-EVE MONCHAMP Master of science (MSc), Université de Montréal, Canada Born on 28.02.1982 Citizen of Canada Accepted on the recommendation of PD Dr. Piet Spaak Dr. Francesco Pomati Prof. Dr. Irene Gregory Eaves Prof. Dr. Jukka Jokela 2017 The major part of this thesis was conducted at the Swiss Federal Institute for Environmental Science and Technology (Eawag/ETH) in the Department of Aquatic Ecology partly in the Department of Surface Water Research and Management in Dübendorf, Switzerland. Financial support was provided by a grand from the Swiss Enlargement Contribution under project IZERZO-142165 (CyanoArchive) to Piet Spaak in the framework of the Romanian- Swiss Research Program. Cover illustration: Photos of sediment cores collected in six peri-alpine lakes that were part of this PhD project. From front to back : (top) Lake Zurich, Hallwilersee, Lake Maggiore; (bottom) Lake Constance, Lake Lugano, Greifensee. 2 Publications This thesis is based on the following papers: 1. Monchamp M-E., Walser J-C., Pomati F., Spaak P. 2016. Sedimentary DNA reveals cyanobacterial community diversity over 200 years in two perialpine lakes, Applied and Environmental Microbiology, 82 (21), 6472 -6482 2. Monchamp M-E., Spaak P., Dubois N., Domaizon I., Bouffard, D., Pomati F. 2017. A century of climate change and eutrophication homogenized lake cyanobacterial communities. (Submitted to Nature Ecology & Evolution) 3. Monchamp M-E., Enache I., Turko P., Pomati F., Rîșnoveanu G., Spaak P. 2017. Sedimentary and egg-bank DNA from 3 European lakes reveal concurrent changes in the composition and diversity of cyanobacterial and Daphnia communities, Hydrobiologia, DOI 10.1007/s10750-017-3247-7 4. Monchamp,M-E., Pomati, F., Spaak, P. The dark side of lakes: diversity and distribution of nonphotosynthetic cyanobacteria. (In preparation) 3 4 Table of contents Summary ............................................................................................................................ 7 Zusammenfassung ............................................................................................................ 9 CHAPTER I : Introduction and thesis outline ..................................................................... 13 CHAPTER II : Sedimentary DNA reveals cyanobacterial community diversity over 200 years in two peri-Alpine lakes ..................................................................................... 31 CHAPTER III: A century of climate change and eutrophication homogenized lake cyanobacterial communities ............................................................................................... 71 CHAPTER IV : Sedimentary and egg-bank DNA from 3 European lakes reveal concurrent changes in the composition and diversity of cyanobacterial and Daphnia communities .................................................................................................................... 103 CHAPTER V : The dark side of lakes: diversity and distribution of nonphotosynthetic cyanobacteria .................................................................................................................. 141 CHAPTER VI : General discussion and outlook ............................................................... 167 Acknowledgements ....................................................................................................... 179 5 6 Summary Anthropogenic global changes have affected almost all ecosystems on Earth and threatened biodiversity worldwide, but the extent of the impact of this pervasive influence is not fully understood. In aquatic ecosystems, eutrophication of lakes has led to the periodic dominance of cyanobacteria, which affects the services that lake ecosystems provide to human society (e.g., tourism, drinking water, fisheries), and sometimes directly threatens the health of animals, including humans. Many lakes in the European peri-Alpine region are regularly affected by the presence of cyanobacteria, but how rapid changes in local and regional lake conditions have contributed to determine their diversity and distribution, for example favouring toxic and bloom-forming taxa, is not well known. Peri-Alpine lakes, with their well-studied eutrophication and climate history, represent excellent study sites for reconstructing past assemblages of planktonic organisms and for investigating their diversity over long time scales of anthropogenic influence by applying molecular techniques to the sedimentary archive. The general aim of this thesis project was to investigate the effects of environmental change, especially climate warming and alteration of nutrient regimes, over the distribution, the biodiversity, and the phylogenetic structure of lacustrine cyanobacterial communities. We used high-throughput sequencing on DNA extracted from dated sediment cores and performed phylogenetic and diversity analyses of the cyanobacterial communities over two centuries to cover the periods of pre-, mid- and post eutrophication of lakes. The first project (Chapter II) was to validate the sedimentary DNA-based reconstruction method by comparing the long-term diversity of cyanobacterial communities recovered from the sediments of two lakes (Greifensee and Lake Zurich) with the diversity assessed by microscopy in water samples collected over four decades as part of lake monitoring programmes. This study confirms the feasibility of the sedimentary DNA approach for assessing the richness and phylogenetic diversity of past communities of cyanobacteria. The second project (Chapter III) was to investigate the biogeography of cyanobacteria and compare their community composition and phylogenetic structure across lakes. For that, the study region was expended to ten lakes across the peri-Alpine area. The results of this project show evidence for the homogenisation of lakes abiotic conditions due to climate warming and eutrophication, and reveal that over the past 150 years, the richness and 7 similarity of cyanobacterial communities has generally increased, particularly gaining buoyant and colonial taxa. The presence of cyanobacteria do not only impair water quality and ecosystem services, but they also have negative effects on other levels of lake food-webs. Chapter IV aims at linking the diversity of Daphnia and cyanobacteria in lakes impacted by anthropogenic eutrophication. This study using the sedimentary Daphnia egg bank and cyanobacterial DNA from two peri-alpine lakes (Switzerland) and a shallow lake in the Danube Biosphere Reserve (Romania) confirms the invasion of D. galeata and the subsequent replacement of native Daphnia lineages by D. galeata taxa in the two Swiss lakes. The results further suggest that D. galeata, D. cucullata, and their sexual descendants appear to have been favoured by the presence of filamentous cyanobacteria at all sites. These results provide novel insights into long-term community interactions between two important plankton groups. During our investigation of cyanobacterial diversity in the sedimentary archive (chapters II & III), we detected two newly described clades of ancestral cyanobacteria called Melainabacteria and ML635J-21. Chapter V presents a short literature review describing these nonphotosynthetic cyanobacteria, and explores their diversity within and across the same ten lakes investigated in chapter II, with the aim to compare their dynamics to the trends observed in cyanobacteria. This study reveals that, unlike cyanobacteria, the richness and composition of nonphotosynthetic cyanobacteria did not vary significantly over the past ~150 years, suggesting that the ladder are not governed by the same environmental factors as the photosynthetic clades. Taken together, the results of these four studies reveal previously unreported patterns in the composition and structure of cyanobacterial communities over broad temporal and spatial scales, and highlight the effects of human-induced environmental changes on cyanobacterial assemblages in freshwater lakes that provide important ecosystem services to humans. Our results support the hypothesis that shifts in the diversity and distribution of taxa might not be reversible even after applying stringent remediation measures for the reduction of water eutrophication, and highlight the importance of increasing our understanding of the underlying mechanisms that regulate community structure to gain predictive ability for future lake management purposes. 8 Zusammenfassung Die globale und anthropogen verursachte Umweltkrise beeinflusst praktisch alle Ökosysteme der Erde und bedroht weltweit die Biodiversität, jedoch ist das Ausmass der Auswirkungen noch nicht vollständig verstanden. Die Eutrophierung in aquatischen Ökosystemen führt zur periodischen Dominanz der Cyanobakterien und diese beeinflussen sowohl Ökosystemleistungen, die Seen der menschlichen Gesellschaft liefern (z.B.: Tourismus,
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