Strain-specific metabarcoding reveals rapid evolution of copper tolerance in populations of the coastal diatom Skeletonema marinoi.
adaptation
copper tolerance
diatoms
phytoplankton
strain metabarcoding
strain-selection
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
11 Sep 2023
11 Sep 2023
Historique:
revised:
03
07
2023
received:
04
04
2023
accepted:
14
08
2023
medline:
12
9
2023
pubmed:
12
9
2023
entrez:
12
9
2023
Statut:
aheadofprint
Résumé
Phytoplankton have short generation times, flexible reproduction strategies, large population sizes and high standing genetic diversity, traits that should facilitate rapid evolution under directional selection. We quantified local adaptation of copper tolerance in a population of the diatom Skeletonema marinoi from a mining-exposed inlet in the Baltic Sea and in a non-exposed population 100 km away. We hypothesized that mining pollution has driven evolution of elevated copper tolerance in the impacted population of S. marinoi. Assays of 58 strains originating from sediment resting stages revealed no difference in the average tolerance to copper between the two populations. However, variation within populations was greater at the mining site, with three strains displaying hyper-tolerant phenotypes. In an artificial evolution experiment, we used a novel intraspecific metabarcoding locus to track selection and quantify fitness of all 58 strains during co-cultivation in one control and one toxic copper treatment. As expected, the hyper-tolerant strains enabled rapid evolution of copper tolerance in the mining-exposed population through selection on available strain diversity. Within 42 days, in each experimental replicate a single strain dominated (30%-99% abundance) but different strains dominated the different treatments. The reference population developed tolerance beyond expectations primarily due to slowly developing plastic response in one strain, suggesting that different modes of copper tolerance are present in the two populations. Our findings provide novel empirical evidence that standing genetic diversity of phytoplankton resting stage allows populations to evolve rapidly (20-50 generations) and flexibly on timescales relevant for seasonal bloom progressions.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Stiftelsen Oscar och Lili Lamms Minne
ID : FO2018-0042
Organisme : Svenska Forskningsrådet Formas
ID : 2016-00594
Organisme : Science for Life Laboratory
Organisme : Knut and Alice Wallenberg Foundation
Organisme : SNIC/Uppsala Multidisciplinary Center for Advanced Computational Science
Informations de copyright
© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.
Références
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. https://doi.org/10.1111/1462-2920.15294
Andersson, B., Berglund, O., Filipsson, H. L., Kourtchenko, O., Godhe, A., Johannesson, K., Töpel, M., Pinder, M. I. M., Hoepfner, L., & Rengefors, K. (2023). Dataset: Evolution of copper tolerance in the coastal diatom Skeletonema marinoi. https://snd.gu.se/en/, 2023-47-1 https://doi.org/10.5878/7eww-g857
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. https://doi.org/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. https://doi.org/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, 8, 376-384. https://doi.org/10.1002/lol2.10291
Bazzicalupo, A. L., Ruytinx, J., Ke, Y.-H., Coninx, L., Colpaert, J. V., Nguyen, N. H., Vilgalys, R., & Branco, S. (2020). Fungal heavy metal adaptation through single nucleotide polymorphisms and copy-number variation. Molecular Ecology, 29, 4157-4169. https://doi.org/10.1111/mec.15618
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. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/10.1038/nmeth.3869
Carlson, H. K., Price, M. N., Callaghan, M., Aaring, A., Chakraborty, R., Liu, H., Kuehl, J. V., Arkin, A. P., & 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. https://doi.org/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. https://doi.org/10.1038/nature02945
Collins, S., Rost, B., & Rynearson, T. A. (2014). Evolutionary potential of marine phytoplankton under ocean acidification. Evolutionary Applications, 7, 140-155. https://doi.org/10.1111/eva.12120
Descamps-Julien, B., & Gonzalez, A. (2005). Stable coexistence in a fluctuating environment: An experimental demonstration. Ecology, 86, 2815-2824. https://doi.org/10.1890/04-1700
Falkowski, P. G., & LaRoche, J. (1991). Acclimation to spectral irradiance in algae. Journal of Phycology, 27, 8-14. https://doi.org/10.1111/j.0022-3646.1991.00008.x
Ferrante, M. I., Entrambasaguas, L., Johansson, M., Töpel, M., Kremp, A., Montresor, M., & Godhe, A. (2019). Exploring molecular signs of sex in the marine diatom skeletonema marinoi. Genes, 10, 494. https://doi.org/10.3390/genes10070494
Flowers, J. M., Hazzouri, K. M., Pham, G. M., Rosas, U., Bahmani, T., Khraiwesh, B., Nelson, D. R., Jijakli, K., Abdrabu, R., Harris, E. H., Lefebvre, P. A., Hom, E. F. Y., Salehi-Ashtiani, K., & Purugganan, M. D. (2015). Whole-genome resequencing reveals extensive natural variation in the model green alga Chlamydomonas reinhardtii. The Plant Cell, 27, 2353-2369. https://doi.org/10.1105/tpc.15.00492
Foster, P. L. (1982). Metal resistances of Chlorophyta from rivers polluted by heavy metals. Freshwater Biology, 12, 41-61. https://doi.org/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 of Gymnodinium mikimotoi and Alexandrium minutum in field samples from Southwest India. Marine Biotechnology, 3, 152-162. https://doi.org/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. https://doi.org/10.1098/rstb.2016.0399
Godhe, A., Sjöqvist, C., Sildever, S., Sefbom, J., Harðardóttir, S., Bertos-Fortis, M., Bunse, C., Gross, S., Johansson, E., & Jonsson, P. R. (2016). Physical barriers and environmental gradients cause spatial and temporal genetic differentiation of an extensive algal bloom. Journal of Biogeography, 43(6), 1130-1142. https://doi.org/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. https://doi.org/10.1002/lom3.10226
Guillard, R. R. L. (1975). Culture of phytoplankton for feeding marine invertebrates. In W. L. Smith, & M. H. Chanley (Eds.), Culture of marine invertebrate animals (pp. 29-60). Springer.
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 of the United States of America, 108, 4252-4257. https://doi.org/10.1073/pnas.1013528108
HELCOM. (2010). Hazardous substances in the Baltic Sea. Balt. Sea Environ. Proc. No. 120B., Helsinki Commission, 116. Retrieved from http://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. https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Hutchinson, G. E. (1961). The paradox of the plankton. American Naturalist, 95, 137-145.
Janssens, T. K., Roelofs, D., & Van Straalen, N. M. (2009). Molecular mechanisms of heavy metal tolerance and evolution in invertebrates. Journal of Insect Science, 16, 3-18. https://doi.org/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 from www.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. https://doi.org/10.1038/s41467-022-33634-w
Kashtan, N., Roggensack, S. E., Rodrigue, S., Thompson, J. W., Biller, S. J., Coe, A., Ding, H., Marttinen, P., Malmstrom, R. R., Stocker, R., Follows, M. J., Stepanauskas, R., & Chisholm, S. W. (2014). Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science, 344, 416-420. https://doi.org/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. https://doi.org/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). 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. https://doi.org/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. https://doi.org/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, 346-351. https://doi.org/10.1038/ngeo1441
Macnair, M. R. (1987). Heavy metal tolerance in plants: A model evolutionary system. Trends in Ecology & Evolution, 2, 354-359. https://doi.org/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. https://doi.org/10.1111/nph.17068
Martin, M. (2011). Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet Journal, 17, 10-12. https://doi.org/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. https://doi.org/10.1017/S0967026202003670
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. https://doi.org/10.3354/meps10236
Ning, W., Ghosh, A., Jilbert, T., Slomp, C. P., Khan, M., Nyberg, J., Conley, D. 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(4), 319-338. https://doi.org/10.1007/s10933-016-9882-6
Ning, W., Nielsen, A., Ivarsson, L. N., Jilbert, T., Åkesson, C., Slomp, C., Andrén, E., Broström, A., & Filipsson, H. (2018). Anthropogenic and climatic impacts on a coastal environment in the Baltic Sea over the last 1000 years. Anthropocene, 21, 66-79. https://doi.org/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. https://doi.org/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. https://doi.org/10.1146/annurev.es.23.110192.001403
Osuna-Cruz, C. M., Bilcke, G., Vancaester, E., De Decker, S., Bones, A. M., Winge, P., Poulsen, N., Bulankova, P., Verhelst, B., Audoor, S., Belisova, D., Pargana, A., Russo, M., Stock, F., Cirri, E., Brembu, T., Pohnert, G., Piganeau, G., Ferrante, M. I., … Vandepoele, K. (2020). The Seminavis robusta genome provides insights into the evolutionary adaptations of benthic diatoms. Nature Communications, 11, 3320. https://doi.org/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. https://doi.org/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, 2023.03.16.532925. https://doi.org/10.1101/2023.03.16.532925
Pinseel, E., Nakov, T., Van den Berge, K., Downey, K. M., Judy, K. J., Kourtchenko, O., Kremp, A., Ruck, E. C., Sjöqvist, C., Töpel, M., Godhe, A., & Alverson, A. J. (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. https://doi.org/10.1038/s41396-022-01230-x
R Core Team. (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing. https://www.R-project.org/
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. https://doi.org/10.1093/plankt/fbw098
Reusch, T. B., & Boyd, P. W. (2013). Experimental evolution meets marine phytoplankton. Evolution, 67, 1849-1859. https://doi.org/10.1111/evo.12035
Reusch, T. B., Dierking, J., Andersson, H. C., Bonsdorff, E., Carstensen, J., Casini, M., Czajkowski, M., Hasler, B., Hinsby, K., Hyytiäinen, K., Johannesson, K., Jomaa, S., Jormalainen, V., Kuosa, H., Kurland, S., Laikre, L., MacKenzie, B. R., Margonski, P., Melzner, F., … Zandersen, M. (2018). The Baltic Sea as a time machine for the future coastal ocean. Science Advances, 4, eaar8195. https://doi.org/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. https://doi.org/10.1038/ncomms1314
Ritz, C., Baty, F., Streibig, J. C., & Gerhard, D. (2015). Dose-response analysis using R. PLoS ONE, 10, e0146021. https://doi.org/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. https://doi.org/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. https://doi.org/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. https://doi.org/10.1016/j.hal.2014.11.001
Schaum, C.-E., Barton, S., Bestion, E., Buckling, A., Garcia-Carreras, B., Lopez, P., Lowe, C., Pawar, S., Smirnoff, N., Trimmer, M., & Yvon-Durocher, G. (2017). Adaptation of phytoplankton to a decade of experimental warming linked to increased photosynthesis. Nature Ecology & Evolution, 1, 1-7. https://doi.org/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. https://doi.org/10.1038/s41467-018-03906-5
Schaum, C. E., & Collins, S. (2014). Plasticity predicts evolution in a marine alga. Proceedings of the Royal Society B: Biological Sciences, 281, 20141486. https://doi.org/10.1098/rspb.2014.1486
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. https://doi.org/10.1038/ismej.2015.102
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. https://doi.org/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, 1024-1030.
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.
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. https://doi.org/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. https://doi.org/10.1111/mec.13208
Sjöqvist, C., Kremp, A., Lindehoff, E., Båmstedt, U., Egardt, J., Gross, S., Jönsson, M., Larsson, H., Pohnert, G., Richter, H., Selander, E., & Godhe, A. (2014). Effects of grazer presence on genetic structure of a phenotypically diverse diatom population. Microbial Ecology, 67, 83-95. https://doi.org/10.1007/s00248-013-0327-8
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. https://doi.org/10.1080/11035899609546323
Sunda, W. (2012). Feedback interactions between trace metal nutrients and phytoplankton in the ocean. Frontiers in Microbiology, 3, 204. https://doi.org/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. https://doi.org/10.1038/s41396-018-0216-8
Tatters, A. O., Roleda, M. Y., Schnetzer, A., Fu, F., Hurd, C. L., Boyd, P. W., Caron, D. A., Lie, A. A. Y., Hoffmann, L. J., & 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. https://doi.org/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. https://doi.org/10.1016/j.ijantimicag.2009.12.017
Waldron, K. J., & Robinson, N. J. (2009). How do bacterial cells ensure that metalloproteins get the correct metal? Nature Reviews: Microbiology, 7, 25-35. https://doi.org/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. https://doi.org/10.1111/gcb.14675
Wood, A. M., Everroad, R., & Wingard, L. (2005). Measuring growth rates in microalgal cultures. In R. A. Andersen (Ed.), Algal culturing techniques (pp. 269-288). 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. https://doi.org/10.1534/genetics.117.201285