References
Ajani, P. A., Petrou, K., Larsson, M. E., Nielsen, D. A., Burke, J., & Murray, S. A. (2020). Phenotypic trait variability as an indication of adaptive capacity in a cosmopolitan marine diatom. Environmental Microbiology, 23 , 207–223. doi:10.1111/1462-2920.15294
Andersson, B., Berglund, O., Filipsson, H. L., Kourtchenko, O., Godhe, A., Johannesson, K., . . . Rengefors, K. (2023). Dataset: Evolution of copper tolerance in the coastal diatom Skeletonema marinoi.https://snd.gu.se/en/, 2023-47 . doi:Included upon acceptance
Andersson, B., Godhe, A., Filipsson, H. L., Rengefors, K., & Berglund, O. (2020). Differences in metal tolerance among strains, populations, and species of marine diatoms-importance of exponential growth for quantification. Aquatic Toxicology, 226 , 105551. doi:10.1016/j.aquatox.2020.105551.
Andersson, B., Godhe, A., Filipsson, H. L., Zetterholm, L., Edler, L., Berglund, O., & Rengefors, K. (2022). Intraspecific variation in metal tolerance modulate competition between two marine diatoms. The ISME journal, 16 , 511–520. doi:10.1038/s41396-021-01092-9
Andersson, B., Rengefors, K., Kourtchenko, O., Johannesson, K., Berglund, O., & Filipsson, H. L. (2023). Cross-contamination risks in sediment-based resurrection studies of phytoplankton. Limnology and Oceanography Letters . doi:10.1002/lol2.10291
Barrett, R. D., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23 , 38-44.
Bazzicalupo, A. L., Ruytinx, J., Ke, Y.-H., Coninx, L., Colpaert, J. V., Nguyen, N. H., . . . Branco, S. (2020). Fungal heavy metal adaptation through single nucleotide polymorphisms and copy-number variation.Molecular Ecology, 29 , 4157-4169. doi:10.1111/mec.15618
Blanc-Mathieu, R., Krasovec, M., Hebrard, M., Yau, S., Desgranges, E., Martin, J., . . . Donnadieu, C. (2017). Population genomics of picophytoplankton unveils novel chromosome hypervariability.Science advances, 3 , e1700239. doi:10.1126/sciadv.1700239
Blanck, H. (2002). A critical review of procedures and approaches used for assessing pollution-induced community tolerance (PICT) in biotic communities. Human and Ecological Risk Assessment, 8 , 1003-1034. doi:10.1080/1080-700291905792
Blanck, H., & Dahl, B. (1996). Pollution-induced community tolerance (PICT) in marine periphyton in a gradient of tri-n-butyltin (TBT) contamination. Aquatic Toxicology, 35 , 59-77. doi:10.1016/0166-445X(96)00007-0
Bushnell, B., Rood, J., & Singer, E. (2017). BBMerge–accurate paired shotgun read merging via overlap. PloS one, 12 , e0185056. doi:10.1371/journal.pone.0185056
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016). DADA2: High-resolution sample inference from Illumina amplicon data. Nature Methods, 13 , 581-583. doi:10.1038/nmeth.3869
Carlson, H. K., Price, M. N., Callaghan, M., Aaring, A., Chakraborty, R., Liu, H., . . . Deutschbauer, A. M. (2019). The selective pressures on the microbial community in a metal-contaminated aquifer. The ISME journal, 13 , 937-949.
Collins, S. (2011). Competition limits adaptation and productivity in a photosynthetic alga at elevated CO2. Proceedings of the Royal Society of London. Series B: Biological Sciences, 278 , 247-255. doi:10.1098/rspb.2010.1173
Collins, S., & Bell, G. (2004). Phenotypic consequences of 1,000 generations of selection at elevated CO2 in a green alga. Nature, 431 , 566-569. doi:10.1038/nature02945
Collins, S., Rost, B., & Rynearson, T. A. (2014). Evolutionary potential of marine phytoplankton under ocean acidification. Evol Appl, 7 , 140-155. doi:10.1111/eva.12120
Descamps-Julien, B., & Gonzalez, A. (2005). Stable coexistence in a fluctuating environment: an experimental demonstration. Ecology, 86 , 2815-2824. doi:10.1890/04-1700
Falkowski, P. G., & LaRoche, J. (1991). Acclimation to spectral irradiance in algae. Journal of Phycology, 27 , 8-14. doi:10.1111/j.0022-3646.1991.00008.x
Flowers, J. M., Hazzouri, K. M., Pham, G. M., Rosas, U., Bahmani, T., Khraiwesh, B., . . . Harris, E. H. (2015). Whole-genome resequencing reveals extensive natural variation in the model green algaChlamydomonas reinhardtii . The Plant Cell, 27 , 2353-2369. doi:10.1105/tpc.15.00492
Foster, P. L. (1982). Metal resistances of Chlorophyta from rivers polluted by heavy metals. Freshwater Biology, 12 , 41-61. doi:10.1111/j.1365-2427.1982.tb00602.x
Godhe, A., Otta, S. K., Rehnstam-Holm, A. S., Karunasagar, I., & Karunasagar, I. (2001). Polymerase chain reaction in detection ofGymnodinium mikimotoi and Alexandrium minutum in field samples from southwest India. Marine Biotechnology, 3 , 152-162. doi:10.1007/s101260000052
Godhe, A., & Rynearson, T. (2017). The role of intraspecific variation in the ecological and evolutionary success of diatoms in changing environments. Philosophical Transactions of the Royal Society B: Biological Sciences, 372 , 20160399. doi:10.1098/rstb.2016.0399
Godhe, A., Sjöqvist, C., Sildever, S., Sefbom, J., Harðardóttir, S., Bertos‐Fortis, M., . . . Jonsson, P. R. (2016). Physical barriers and environmental gradients cause spatial and temporal genetic differentiation of an extensive algal bloom. Journal of Biogeography, 43 , 1130-1142. doi:10.1111/jbi.12722
Grangeteau, C., David, V., Hervé, A., Guilloux-Benatier, M., & Rousseaux, S. (2017). The sensitivity of yeasts and yeasts-like fungi to copper and sulfur could explain lower yeast biodiversity in organic vineyards. FEMS Yeast Research, 17 , fox092.
Gresham, D., & Dunham, M. J. (2014). The enduring utility of continuous culturing in experimental evolution. Genomics, 104 , 399-405.
Gross, S., Kourtchenko, O., Rajala, T., Andersson, B., Fernandez, L., Blomberg, A., & Godhe, A. (2017). Optimization of a high‐throughput phenotyping method for chain‐forming phytoplankton species.Limnology and Oceanography: Methods, 16 , 57-67 doi:10.1002/lom3.10226
HELCOM. (2010). Hazardous substances in the Baltic Sea. Balt. Sea Environ. Proc. No. 120B. , Helsinki Commission,116. Retrieved fromhttp://www.helcom.fi/Lists/Publications/BSEP120B.pdf
Hillebrand, H., Dürselen, C. D., Kirschtel, D., Pollingher, U., & Zohary, T. (1999). Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology, 35 , 403-424. doi:10.1046/j.1529-8817.1999.3520403.x
Hutchinson, G. E. (1961). The paradox of the plankton. American Naturalist, 95 , 137-145.
Härnström, K., Ellegaard, M., Andersen, T. J., & Godhe, A. (2011). Hundred years of genetic structure in a sediment revived diatom population. Proceedings of the National Academy of Sciences, USA, 108 , 4252–4257. doi:10.1073/pnas.1013528108
Janssens, T. K., Roelofs, D., & Van Straalen, N. M. (2009). Molecular mechanisms of heavy metal tolerance and evolution in invertebrates.Insect Science, 16 , 3-18. doi:10.1111/j.1744-7917.2009.00249.x
Kalinowska, R., & Pawlik-Skowrońska, B. (2008). Metal resistance of soil algae (Chlorophyta) occurring in post-flotation Zn/Pb-and Cu-tailing ponds. Polish Journal of Ecology, 56 , 415-430.
Karlsson, M., Malmaeus, M., Rydin, E., & Jonsson, P. (2010). Bottenundersökningar i Upplands, Stockholms, Södermanlands och Östergötlands skärgårdar 2008-2009. Rapport B1928, IVL Svenska Miljöinstitutet, Stockholm . Retrieved fromwww.ivl.se
Karve, S., & Wagner, A. (2022). Environmental complexity is more important than mutation in driving the evolution of latent novel traits in E. coli . Nature Communications, 13 , 5904. doi:10.1038/s41467-022-33634-w
Kashtan, N., Roggensack, S. E., Rodrigue, S., Thompson, J. W., Biller, S. J., Coe, A., . . . Chisholm, S. W. (2014). Single-cell genomics reveals hundreds of coexisting subpopulations in wildProchlorococcus . Science, 344 , 416-420. doi:10.1126/science.1248575
Kerfoot, W. C., Robbins, J. A., & Weider, L. J. (1999). A new approach to historical reconstruction: combining descriptive and experimental paleolimnology. Limnology and Oceanography, 44 , 1232–1247. doi:10.4319/lo.1999.44.5.1232
Kimura, M. (1983). The neutral theory of molecular evolution : Cambridge University Press.
Lehtonen, K. K., Bignert, A., Bradshaw, C., Broeg, K., & Schiedek, D. (2017). Chemical pollution and ecotoxicology. In P. S. Snoeijs-Leijonmalm, H.: & T. Radziejewska (Eds.), Biological Oceanography of the Baltic Sea (pp. 547-589). Dordrecht, The Netherlands: Springer Nature.
Lemire, J. A., Harrison, J. J., & Turner, R. J. (2013). Antimicrobial activity of metals: mechanisms, molecular targets and applications.Nature Reviews Microbiology, 11 , 371-384. doi:10.1038/nrmicro3028
Lewis, J., Harris, A. S. D., Jones, K. J., & Edmonds, R. L. (1999). Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. Journal of Plankton Research, 21 , 343–354. doi:10.1080/00071618000650361
Lohbeck, K. T., Riebesell, U., & Reusch, T. B. (2012). Adaptive evolution of a key phytoplankton species to ocean acidification.Nature Geoscience, 5 , 346. doi:10.1038/ngeo1441
Macnair, M. R. (1987). Heavy metal tolerance in plants: A model evolutionary system. Trends in Ecology & Evolution, 2 , 354-359. doi:10.1016/0169-5347(87)90135-2
Malerba, M. E., Marshall, D. J., Palacios, M. M., Raven, J. A., & Beardall, J. (2020). Cell size influences inorganic carbon acquisition in artificially selected phytoplankton. New Phytologist, 229 , 2647-2659. doi:10.1111/nph.17068
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. journal, 17 , 10-12. doi:10.14806/ej.17.1.200
McQuoid, M. R., Godhe, A., & Nordberg, K. (2002). Viability of phytoplankton resting stages in the sediments of a coastal Swedish fjord. European Journal of Phycology, 37 , 191–201. doi:10.1017/S0967026202003670
Mock, T., Otillar, R. P., Strauss, J., McMullan, M., Paajanen, P., Schmutz, J., . . . Grigoriev, I. V. (2017). Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus . Nature, 541 , 536-540. doi:10.1038/nature20803
Montresor, M., Di Prisco, C., Sarno, D., Margiotta, F., & Zingone, A. (2013). Diversity and germination patterns of diatom resting stages at a coastal Mediterranean site. Marine Ecology Progress Series, 484 , 79–95. doi:10.3354/meps10236
Ning, W., Ghosh, A., Jilbert, T., Slomp, C. P., Khan, M., Nyberg, J., . . . Filipsson, H. L. (2016). Evolving coastal character of a Baltic Sea inlet during the Holocene shoreline regression: impact on coastal zone hypoxia. Journal of Paleolimnology, 55 , 319–338. doi:10.1007/s10933-016-9882-6
Ning, W., Nielsen, A., Ivarsson, L. N., Jilbert, T., Åkesson, C., Slomp, C., . . . Filipsson, H. (2018). Anthropogenic and climatic impacts on a coastal environment in the Baltic Sea over the last 1000 years.Anthropocene, 21 , 66–79. doi:10.1016/j.ancene.2018.02.003
Ning, W., Tang, J., & Filipsson, H. L. (2016). Long-term coastal openness variation and its impact on sediment grain-size distribution: a case study from the Baltic Sea. Earth Surface Dynamics, 4 , 773–780. doi:10.5194/esurf-4-773-2016
OECD. (2006). Test No. 201: Alga, Growth Inhibition Test. Retrived from: https://www.oecd-ilibrary.org/content/publication/9789264069923-en..
Ohta, T. (1992). The Nearly Neutral Theory of Molecular Evolution.Annual Review of Ecology and Systematics, 23 , 263-286. doi:10.1146/annurev.es.23.110192.001403
Osuna-Cruz, C. M., Bilcke, G., Vancaester, E., De Decker, S., Bones, A. M., Winge, P., . . . Audoor, S. (2020). The Seminavis robustagenome provides insights into the evolutionary adaptations of benthic diatoms. Nature Communications, 11 , 3320. doi:10.1038/s41467-020-17191-8
Pesce, S., Lissalde, S., Lavieille, D., Margoum, C., Mazzella, N., Roubeix, V., & Montuelle, B. (2010). Evaluation of single and joint toxic effects of diuron and its main metabolites on natural phototrophic biofilms using a pollution-induced community tolerance (PICT) approach.Aquatic Toxicology, 99 , 492-499. doi:10.1016/j.aquatox.2010.06.006
Pinder, M. I. M., Andersson, B., Rengefors, K., Blossom, H. B., Svensson, M., & Töpel, M. (2023). Bamboozle: A bioinformatic tool for identification and quantification of intraspecific barcodes.bioRxiv . doi:10.1101/2023.03.16.532925
Pinseel, E., Nakov, T., Van den Berge, K., Downey, K. M., Judy, K. J., Kourtchenko, O., . . . Töpel, M. (2022). Strain-specific transcriptional responses overshadow salinity effects in a marine diatom sampled along the Baltic Sea salinity cline. The ISME journal, 16 , 1776–1787. doi:10.1038/s41396-022-01230-x
Read, B. A., Kegel, J., Klute, M. J., Kuo, A., Lefebvre, S. C., Maumus, F., . . . Salamov, A. (2013). Pan genome of the phytoplanktonEmiliania underpins its global distribution. Nature, 499 , 209-213. doi:10.1038/nature12221
Rengefors, K., Kremp, A., Reusch, T. B., & Wood, A. M. (2017). Genetic diversity and evolution in eukaryotic phytoplankton: revelations from population genetic studies. Journal of Plankton Research, 39 , 165-179. doi:10.1093/plankt/fbw098
Reusch, T. B., & Boyd, P. W. (2013). Experimental evolution meets marine phytoplankton. Evolution, 67 , 1849-1859. doi:10.1111/evo.12035
Reusch, T. B., Dierking, J., Andersson, H. C., Bonsdorff, E., Carstensen, J., Casini, M., . . . Hyytiäinen, K. (2018). The Baltic Sea as a time machine for the future coastal ocean. Science advances, 4 , eaar8195. doi:10.1126/sciadv.aar8195
Ribeiro, S., Berge, T., Lundholm, N., Andersen, T. J., Abrantes, F., & Ellegaard, M. (2011). Phytoplankton growth after a century of dormancy illuminates past resilience to catastrophic darkness. Nature Communications, 2 , 311. doi:10.1038/ncomms1314
Ritz, C., Baty, F., Streibig, J. C., & Gerhard, D. (2015). Dose-response analysis using R. PloS one, 10 , e0146021. doi:10.1371/journal.pone.0146021
Robinson, D. G., Chen, W., Storey, J. D., & Gresham, D. (2014). Design and analysis of Bar-seq experiments. G3: Genes, Genomes, Genetics, 4 , 11-18. doi:10.1534/g3.113.008565
Sassenhagen, I., Erdner, D., Lougheed, B., Richlen, M., & Sjöqvist, C. (2021). Estimating proportion of clones and genotype richness in aquatic microalgae. Authorea Preprints . doi:10.22541/au.161876383.32271114/v1
Sassenhagen, I., Wilken, S., Godhe, A., & Rengefors, K. (2015). Phenotypic plasticity and differentiation in an invasive freshwater microalga. Harmful Algae, 41 , 38-45. doi:10.1016/j.hal.2014.11.001
Schaum, C.-E., Barton, S., Bestion, E., Buckling, A., Garcia-Carreras, B., Lopez, P., . . . Trimmer, M. (2017). Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis.Nature Ecology & Evolution, 1 , 1-7. doi:10.1038/s41559-017-0094
Schaum, C.-E., Buckling, A., Smirnoff, N., Studholme, D., & Yvon-Durocher, G. (2018). Environmental fluctuations accelerate molecular evolution of thermal tolerance in a marine diatom.Nature Communications, 9 , 1719. doi:10.1038/s41467-018-03906-5
Schaum, C.-E., Rost, B., & Collins, S. (2016). Environmental stability affects phenotypic evolution in a globally distributed marine picoplankton. The ISME journal, 10 , 75-84. doi:10.1038/ismej.2015.102
Schaum, C. E., & Collins, S. (2014). Plasticity predicts evolution in a marine alga. Proceedings of the Royal Society B: Biological Sciences, 281 , 20141486. doi:doi:10.1098/rspb.2014.1486
Scheinin, M., Riebesell, U., Rynearson, T. A., Lohbeck, K. T., & Collins, S. (2015). Experimental evolution gone wild. Journal of the Royal Society Interface, 12 , 20150056. doi:10.1098/rsif.2015.0056
Schlüter, L., Lohbeck, K. T., Gutowska, M. A., Gröger, J. P., Riebesell, U., & Reusch, T. B. (2014). Adaptation of a globally important coccolithophore to ocean warming and acidification. Nature Climate Change, 4 , 1024.
Schmitt, H., Haapakangas, H., & van Beelen, P. (2005). Effects of antibiotics on soil microorganisms: time and nutrients influence pollution-induced community tolerance. Soil Biology and Biochemistry, 37 , 1882-1892.
Schreiber, U. (1998). Chlorophyll fluorescence: New Instruments for Special Applications. In G. Garab (Ed.), Photosynthesis: mechanisms and effects (pp. 4253-4258). Springer, Dordrecht: Springer.
Sefbom, J., Kremp, A., Rengefors, K., Jonsson, P. R., Sjoqvist, C., & Godhe, A. (2018). A planktonic diatom displays genetic structure over small spatial scales. Environmental Microbiology, 20 , 2783-2795. doi:10.1111/1462-2920.14117
Sjöqvist, C., Godhe, A., Jonsson, P. R., Sundqvist, L., & Kremp, A. (2015). Local adaptation and oceanographic connectivity patterns explain genetic differentiation of a marine diatom across the North Sea-Baltic Sea salinity gradient. Molecular Ecology, 24 , 2871-2885. doi:10.1111/mec.13208
Sjöqvist, C., Kremp, A., Lindehoff, E., Båmstedt, U., Egardt, J., Gross, S., . . . Richter, H. (2014). Effects of grazer presence on genetic structure of a phenotypically diverse diatom population. Microbial Ecology, 67 , 83-95. doi:10.1007/s00248-013-0327-8
Sunda, W. (2012). Feedback Interactions between Trace Metal Nutrients and Phytoplankton in the Ocean. Frontiers in Microbiology, 3 , 204. doi:10.3389/fmicb.2012.00204
Sundqvist, L., Godhe, A., Jonsson, P. R., & Sefbom, J. (2018). The anchoring effect-long-term dormancy and genetic population structure.The ISME journal, 12 , 2929-2941. doi:10.1038/s41396-018-0216-8
Söderhielm, J., & Sundblad, K. (1996). The Solstad Cu‐Co‐Au mineralization and its relation to post‐Svecofennian regional shear zones in southeastern Sweden. GFF, 118 , 47-47. doi:10.1080/11035899609546323
Tatters, A. O., Roleda, M. Y., Schnetzer, A., Fu, F., Hurd, C. L., Boyd, P. W., . . . Hutchins, D. A. (2013). Short-and long-term conditioning of a temperate marine diatom community to acidification and warming.Philosophical Transactions of the Royal Society B: Biological Sciences, 368 , 20120437. doi:10.1098/rstb.2012.0437
Tupin, A., Gualtieri, M., Roquet-Banères, F., Morichaud, Z., Brodolin, K., & Leonetti, J.-P. (2010). Resistance to rifampicin: at the crossroads between ecological, genomic and medical concerns.International Journal of Antimicrobial Agents, 35 , 519-523. doi:10.1016/j.ijantimicag.2009.12.017
Vancaester, E., Depuydt, T., Osuna-Cruz, C. M., & Vandepoele, K. (2020). Comprehensive and Functional Analysis of Horizontal Gene Transfer Events in Diatoms. Molecular Biology and Evolution, 37 , 3243-3257. doi:10.1093/molbev/msaa182
Waldron, K. J., & Robinson, N. J. (2009). How do bacterial cells ensure that metalloproteins get the correct metal? Nature Reviews: Microbiology, 7 , 25. doi:10.1038/nrmicro2057
Wolf, K. K., Romanelli, E., Rost, B., John, U., Collins, S., Weigand, H., & Hoppe, C. J. (2019). Company matters: The presence of other genotypes alters traits and intraspecific selection in an Arctic diatom under climate change. Global Change Biology, 25 , 2869-2884. doi:10.1111/gcb.14675
Wood, A. M., Everroad, R., & Wingard, L. (2005). Measuring growth rates in microalgal cultures, p. 269-288. Andersen, R. A. (Ed.): Algal culturing techniques. Elsevier.
Xu, C., Sun, T., Li, S., Chen, L., & Zhang, W. (2018). Adaptive laboratory evolution of cadmium tolerance in Synechocystis sp. PCC 6803.Biotechnology for biofuels, 11 , 1-15.
Zhao, Y., Dominska, M., Petrova, A., Bagshaw, H., Kokoska, R. J., & Petes, T. D. (2017). Properties of mitotic and meiotic recombination in the tandemly-repeated CUP1 gene cluster in the yeast Saccharomyces cerevisiae . Genetics, 206 , 785-800. doi:10.1534/genetics.117.201285
Tables
Table 1: Summary of key observations during the artificial evolution experiment on a replicate-by-replicate basis. Several barcode samples at day 42 were cross-contaminated during the library preparation and have been omitted from further quantitative analysis (see Fig S4 for more details). RO5AC is a mono-clonal strain run as a reference control between the two populations experiments. Abbreviations: C; control treatment, Cu; copper treatment, GP; Gropviken [reference inlet], VG; Gåsfjärden [mining inlet]