Show simple item record

Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa

dc.contributor.authorJackrel, Sara L.
dc.contributor.authorWhite, Jeffrey D.
dc.contributor.authorEvans, Jacob T.
dc.contributor.authorBuffin, Kyle
dc.contributor.authorHayden, Kristen
dc.contributor.authorSarnelle, Orlando
dc.contributor.authorDenef, Vincent J.
dc.date.accessioned2019-10-30T15:30:33Z
dc.date.availableWITHHELD_12_MONTHS
dc.date.available2019-10-30T15:30:33Z
dc.date.issued2019-09
dc.identifier.citationJackrel, Sara L.; White, Jeffrey D.; Evans, Jacob T.; Buffin, Kyle; Hayden, Kristen; Sarnelle, Orlando; Denef, Vincent J. (2019). "Genome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa." Molecular Ecology 28(17): 3994-4011.
dc.identifier.issn0962-1083
dc.identifier.issn1365-294X
dc.identifier.urihttps://hdl.handle.net/2027.42/151861
dc.description.abstractIntraspecific niche divergence is an important driver of species range, population abundance and impacts on ecosystem functions. Genetic changes are the primary focus when studying intraspecific divergence; however, the role of ecological interactions, particularly host‐microbiome symbioses, is receiving increased attention. The relative importance of these evolutionary and ecological mechanisms has seen only limited evaluation. To address this question, we used Microcystis aeruginosa, the globally distributed cyanobacterium that dominates freshwater harmful algal blooms. These blooms have been increasing in occurrence and intensity worldwide, causing major economic and ecological damages. We evaluated 46 isolates of M. aeruginosa and their microbiomes, collected from 14 lakes in Michigan, USA, that vary over 20‐fold in phosphorus levels, the primary limiting nutrient in freshwater systems. Genomes of M. aeruginosa diverged along this phosphorus gradient in genomic architecture and protein functions. Fitness in low‐phosphorus lakes corresponded with additional shifts within M. aeruginosa including genome‐wide reductions in nitrogen use, an expansion of phosphorus assimilation genes and an alternative life history strategy of nonclonal colony formation. In addition to host shifts, despite culturing in common‐garden conditions, host‐microbiomes diverged along the gradient in taxonomy, but converged in function with evidence of metabolic interdependence between the host and its microbiome. Divergence corresponded with a physiological trade‐off between fitness in low‐phosphorus environments and growth rate in phosphorus‐rich conditions. Co‐occurrence of genotypes adapted to different nutrient environments in phosphorus‐rich lakes may have critical implications for understanding how M. aeruginosa blooms persist after initial nutrient depletion. Ultimately, we demonstrate that the intertwined effects of genome evolution, host life history strategy and ecological interactions between a host and its microbiome correspond with an intraspecific niche shift with important implications for whole ecosystem function.
dc.publisherWiley Periodicals, Inc.
dc.publisherCambridge University Press
dc.subject.otheradaptation
dc.subject.othercyanobacterial harmful algal blooms
dc.subject.othergenome evolution
dc.subject.otherhost‐microbiome
dc.subject.otherintraspecific variation
dc.subject.othernutrient limitation
dc.titleGenome evolution and host‐microbiome shifts correspond with intraspecific niche divergence within harmful algal bloom‐forming Microcystis aeruginosa
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/1/mec15198_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/2/mec15198.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/151861/3/mec15198-sup-0001-Supinfo.pdf
dc.identifier.doi10.1111/mec.15198
dc.identifier.sourceMolecular Ecology
dc.identifier.citedreferenceSarnelle, O. ( 1992 ). Contrasting effects of Daphnia ratios of nitrogen to phosphorus in a eutrophic, hard‐water lake. Limnology and Oceanography, 37, 1527 – 1542.
dc.identifier.citedreferenceSchloss, P. D., Westcott, S. L., Ryabin, T., Hall, J. R., Hartmann, M., Hollister, E. B., … Weber, C. F. ( 2009 ). Introducing mothur: Open‐source, platform‐independent, community‐supported software for describing and comparing microbial communities. Applied and Environmental Microbiology, 75, 7537 – 7541. https://doi.org/10.1128/AEM.01541-09
dc.identifier.citedreferenceSchwarz, R., & Grossman, A. R. ( 1998 ). A response regulator of cyanobacteria integrates diverse environmental signals and is critical for survival under extreme conditions. Proceedings of the National Academy of Sciences of the United States of America, 95 ( 18 ), 11008 – 11013.
dc.identifier.citedreferenceSebastian, M., & Ammerman, J. W. ( 2009 ). The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME Journal, 3, 563. https://doi.org/10.1038/ismej.2009.10
dc.identifier.citedreferenceSeip, K. L., & Reynolds, C. S. ( 1995 ). Phytoplankton functional attributes along trophic gradient and season. Limnology and Oceanography, 40, 589 – 597. https://doi.org/10.4319/lo.1995.40.3.0589
dc.identifier.citedreferenceSeymour, J. R., Amin, S. A., Raina, J., & Stocker, R. ( 2017 ). Zooming in on the phycosphere: The ecological interface for phytoplankton–bacteria relationships. Nature Microbiology, 2, 17065. https://doi.org/10.1038/nmicrobiol.2017.65
dc.identifier.citedreferenceShapiro, B. J., & Polz, M. F. ( 2014 ). Ordering microbial diversity into ecologically and genetically cohesive units. Trends in Microbiology, 22, 235 – 247. https://doi.org/10.1016/j.tim.2014.02.006
dc.identifier.citedreferenceSmith, R. J. ( 2017 ). Solutions for loss of information in high‐beta‐diversity community data. Methods in Ecology and Evolution, 8, 68 – 74. https://doi.org/10.1111/2041-210X.12652
dc.identifier.citedreferenceSoranno, P. A., Bacon, L. C., Beauchene, M., Bednar, K. E., Bissell, E. G., Boudreau, C. K., … Yuan, S. ( 2017 ). LAGOS‐NE: A multi‐scaled geospatial and temporal database of lake ecological context and water quality for thousands of US lakes. GigaScience, 6, 12. https://doi.org/10.1093/gigascience/gix101
dc.identifier.citedreferenceStamatakis, A. ( 2006 ). RAxML‐VI‐HPC: Maximum likelihood‐based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688 – 2690. https://doi.org/10.1093/bioinformatics/btl446
dc.identifier.citedreferenceSteffen, M. M., Davis, T. W., McKay, R. M. L., Bullerjahn, G. S., Krausfeldt, L. E., Stough, J. M. A., … Wilhelm, S. W. ( 2017 ). Ecophysiological examination of the Lake Erie Microcystis bloom in 2014: Linkages between biology and the water supply shutdown of Toledo, OH. Environmental Science and Technology, 51, 6745 – 6755.
dc.identifier.citedreferenceSterner, R. W. ( 2008 ). On the phosphorus limitation paradigm of lakes. International Review of Hydrology, 93, 433 – 445.
dc.identifier.citedreferenceStrom, S., Bright, K., Fredrickson, K., & Brahamsha, B. ( 2017 ). The Synechococcus cell surface protein SwmA increases vulnerability to predation by flagellates and ciliates. Limnology and Oceanography, 62, 784 – 794.
dc.identifier.citedreferenceTanabe, Y., Okazaki, Y., Yoshida, M., Matsuura, H., Kai, A., Shiratori, T., … Watanabe, M. M. ( 2015 ). A novel alphaproteobacterial ectosymbiont promotes the growth of the hydrocarbon‐rich green alga Botryococcus braunii. Scientific Reports, 5, 10467. https://doi.org/10.1038/srep10467
dc.identifier.citedreferenceTreangen, T. J., & Salzberg, S. L. ( 2012 ). Repetitive DNA and next‐generation sequencing: Computational challenges and solutions. Nature Reviews Genetics, 13, 36 – 46. https://doi.org/10.1038/nrg3117
dc.identifier.citedreferenceTurnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., … Gordon, J. I. ( 2009 ). A core gut microbiome in obese and lean twins. Nature, 457, 480 – 484. https://doi.org/10.1038/nature07540
dc.identifier.citedreferenceVimr, E. R. ( 1994 ). Microbial sialidases: Does bigger always mean better? Trends in Microbiology, 2, 271 – 277. https://doi.org/10.1016/0966-842X(94)90003-5
dc.identifier.citedreferenceVox, M., Hesselman, M. C., te Beek, T. A., van Passel, M. W. J., & Eyre‐Walker, A. ( 2015 ). Rates of lateral genes transfer in prokaryotes: High but why? Trends in Microbiology, 23, 598 – 605.
dc.identifier.citedreferenceWang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. ( 2007 ). Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Applied and Environmental Microbiology, 5261 – 5267. https://doi.org/10.1128/AEM.00062-07
dc.identifier.citedreferenceWehr, J. D., & Sheath, R. G. ( 2003 ). Freshwater algae of North America: Ecology and classification. San Diego, CA: Academic Press.
dc.identifier.citedreferenceWetzel, R. G. ( 2001 ). Limnology: Lake and river ecosystems ( 3 rd ed.). San Diego, CA: Elsevier Academic Press.
dc.identifier.citedreferenceWhite, J. D., Kaul, R. B., Knoll, L. B., Wilson, A. E., & Sarnelle, O. ( 2011 ). Large variation in vulnerability to grazing within a population of the colonial phytoplankter, Microcystis aeruginosa. Limnology and Oceanography, 56, 1714 – 1724.
dc.identifier.citedreferenceWhitham, T. G., Bailey, J. K., Schweitzer, J. A., Shuster, S. M., Bangert, R. K., LeRoy, C. J., … Wooley, S. C. ( 2006 ). A framework for community and ecosystem genetics: From genes to ecosystems. Nature Reviews Genetics, 7, 510 – 523. https://doi.org/10.1038/nrg1877
dc.identifier.citedreferenceWilson, A. E., Kaul, R. B., & Sarnelle, O. ( 2010 ). Growth rate consequences of coloniality in a harmful phytoplankter. PLoS ONE, 5, e8679. https://doi.org/10.1371/journal.pone.0008679
dc.identifier.citedreferenceWilson, A. E., Sarnelle, O., Neilan, B. A., Salmon, T. P., Gehringer, M. M., & Hay, M. E. ( 2005 ). Genetic variation of the bloom‐forming cyanobacterium Microcystis aeruginosa within and among lakes: Implications for harmful algal blooms. Applied and Environmental Microbiology, 71, 6126 – 6133. https://doi.org/10.1128/AEM.71.10.6126-6133.2005
dc.identifier.citedreferenceWilson, A. E., Wilson, W. A., & Hay, M. E. ( 2006 ). Intraspecific variation in growth and morphology of the bloom‐forming cyanobacterium Microcystis aeruginosa. Applied & Environmental Microbiology, 72, 7386 – 7389. https://doi.org/10.1128/AEM.00834-06
dc.identifier.citedreferenceXiao, M., Li, M., & Reynolds, C. S. ( 2018 ). Colony formation in the cyanobacterium Microcystis. Biological Reviews, 93, 1399 – 1420.
dc.identifier.citedreferenceYanofsky, C., Cox, E. C., & Horn, V. ( 1966 ). The unusual mutagenic specificity of an E. coli mutator gene. Proceedings of the National Academy of Sciences of the United States of America, 55, 274 – 281. https://doi.org/10.1073/pnas.55.2.274
dc.identifier.citedreferenceZippel, B., & Neu, T. R. ( 2011 ). Characterization of glycoconjugates of extracellular polymeric substances in tufa‐associated biofilms by using fluorescence lectin‐binding analysis. Applied and Environmental Microbiology, 77, 505 – 516. https://doi.org/10.1128/AEM.01660-10
dc.identifier.citedreferenceAnantharaman, K., Duhaime, M. B., Breier, J. A., Wendt, K. A., Toner, B. M., & Dick, G. J. ( 2014 ). Sulfur oxidation genes in diverse deep‐sea viruses. Science, 344, 757 – 760. https://doi.org/10.1126/science.1252229
dc.identifier.citedreferenceBaldia, S. F., Evangelista, A. D., Aralar, E. V., & Santiago, A. E. ( 2007 ). Nitrogen and phosphorus utilization in the cyanobacterium Microcystis aeruginosa isolated from Laguna de Bay, Philippines. Journal of Applied Phycology, 19, 607 – 613. https://doi.org/10.1007/s10811-007-9209-0
dc.identifier.citedreferenceBarrett, R. D. H., & Schluter, D. ( 2008 ). Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38 – 44. https://doi.org/10.1016/j.tree.2007.09.008
dc.identifier.citedreferenceBassar, R. D., Marshall, M. C., López‐Sepulcre, A., Zandonà, E., Auer, S. K., Travis, J., … Reznick, D. N. ( 2010 ). Local adaptation in Trinidadian guppies alters ecosystem processes. Proceedings of the National Academy of Sciences of the United States of America, 107, 3616 – 3621. https://doi.org/10.1073/pnas.0908023107
dc.identifier.citedreferenceBenjamini, Y., & Hochberg, Y. ( 1995 ). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B, 57, 289 – 300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
dc.identifier.citedreferenceBergmann, G. T., Bates, S. T., Eilers, K. G., Lauber, C. L., Caporaso, J. G., Walters, W. A., … Fierer, N. ( 2011 ). The under‐recognized dominance of Verrucomicrobia in soil bacterial communities. Soil Biology and Biochemistry, 43, 1450 – 1455. https://doi.org/10.1016/j.soilbio.2011.03.012
dc.identifier.citedreferenceBerry, M. A., Davis, T. W., Cory, R. M., Duhaime, M. B., Johengen, T. H., Kling, G. W., … Denef, V. J. ( 2017 ). Cyanobacterial harmful algal blooms are a biological disturbance to western Lake Erie bacterial communities. Environmental Microbiology, 19, 1149 – 1162.
dc.identifier.citedreferenceBerry, M. A., White, J. D., Davis, T. W., Jain, S., Johengen, T. H., Dick, G. J., … Denef, V. J. ( 2017 ). Are oligotypes meaningful ecological and phylogenetic units? A case study of Microcystis in freshwater lakes. Frontiers in Microbiology, 8, 1 – 7. https://doi.org/10.3389/fmicb.2017.00365
dc.identifier.citedreferenceBolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., … Vasseur, D. A. ( 2011 ). Why intraspecific trait variation matters in community ecology. Trends in Ecology and Evolution, 26, 183 – 192.
dc.identifier.citedreferenceBuchfink, B., Xie, C., & Huson, D. H. ( 2014 ). Fast and sensitive protein alignment using DIAMOND. Nature Methods, 12, 59 – 60. https://doi.org/10.1038/nmeth.3176
dc.identifier.citedreferenceBurkholder, J. M., & Gilbert, P. M. ( 2009 ). The importance of intraspecific variability in harmful algae‐ preface to a collection of topical papers. Harmful Algae, 8, 744 – 745. https://doi.org/10.1016/j.hal.2009.03.006
dc.identifier.citedreferenceCai, H., Jiang, H., Krumholz, L. R., & Yang, Z. ( 2014 ). Bacterial community composition of size‐fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS ONE, 9, e102879. https://doi.org/10.1371/journal.pone.0102879
dc.identifier.citedreferenceChislock, M. F., Sarnelle, O., Olsen, B., Doster, E., & Wilson, A. E. ( 2013 ). Large effects of consumer offense on ecosystem structure and function. Ecology, 94, 2375 – 2380. https://doi.org/10.1890/13-0320.1
dc.identifier.citedreferenceContreras‐Moreira, B., & Vinuesa, P. ( 2013 ). GET_HOMOLOGUES, a versatile software package for scalable and robust microbial pan‐genome analysis. Applied and Environmental Microbiology, 79, 7696 – 7701. https://doi.org/10.1128/AEM.02411-13
dc.identifier.citedreferenceCostas, E., Lopez‐Rodas, V., Javier Toro, F., & Flores‐Moya, A. ( 2008 ). The number of cells in colonies of the cyanobacterium Microcystis aeruginosa satisfies Benford’s Law. Aquatic Botany, 89, 341 – 343. https://doi.org/10.1016/j.aquabot.2008.03.011
dc.identifier.citedreferenceCrump, B. C., Adams, H. E., Hobbie, J. E., & Kling, G. W. ( 2007 ). Biogeography of bacterioplankton in lakes and streams of an arctic tundra catchment. Ecology, 88, 1365 – 1378. https://doi.org/10.1890/06-0387
dc.identifier.citedreferenceCrutsinger, G. M., Collins, M. D., Fordyce, J. A., Gompert, Z., Nice, C. C., & Sanders, N. J. ( 2006 ). Plant genotypic diversity predicts community structure and governs an ecosystem process. Science, 313, 966 – 968. https://doi.org/10.1126/science.1128326
dc.identifier.citedreferenceDeMott, W. R., & Mckinney, E. N. ( 2015 ). Use it or lose it? Loss of grazing defenses during laboratory culture of the digestion‐resistant green alga Oocystis. Journal of Plankton Research, 37, 399 – 408. https://doi.org/10.1093/plankt/fbv013
dc.identifier.citedreferenceDenamur, E., & Matic, I. ( 2006 ). Evolution of mutation rates in bacteria. Molecular Microbiology, 60, 820 – 827. https://doi.org/10.1111/j.1365-2958.2006.05150.x
dc.identifier.citedreferenceDick, G. J., Andersson, A. F., Baker, B. J., Simmons, S. L., Thomas, B. C., Yelton, A. P., & Banfield, J. F. ( 2009 ). Community‐wide analysis of microbial genome sequence signatures. Genome Biology, 10, R85. https://doi.org/10.1186/gb-2009-10-8-r85
dc.identifier.citedreferenceDittami, S. M., Duboscq‐Bidot, L., Perennou, M., Gobet, A., Corre, E., Boyen, C., & Tonon, T. ( 2016 ). Host–microbe interactions as a driver of acclimation to salinity gradients in brown algal cultures. ISME Journal, 10, 51 – 63. https://doi.org/10.1038/ismej.2015.104
dc.identifier.citedreferenceDrake, J. W., Charlesworth, B., Charlesworth, D., & Crow, J. F. ( 1998 ). Rates of spontaneous mutation. Genetics, 148, 1667 – 1686.
dc.identifier.citedreferenceEdgar, R. C. ( 2004 ). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792 – 1797. https://doi.org/10.1093/nar/gkh340
dc.identifier.citedreferenceEigemann, F., Hilt, S., Salka, I., & Grossart, H.‐P. ( 2013 ). Bacterial community composition associated with freshwater algae: Species specificity versus dependency on environmental conditions and source community. FEMS Microbiology Ecology, 32, 650 – 663.
dc.identifier.citedreferenceFranguel, L., Quillardet, P., Castets, A., Humbert, J., Matthijs, H. C. P., Cortez, D., … Tandeau de Marsac, N. ( 2008 ). Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics, 9, 274. https://doi.org/10.1186/1471-2164-9-274
dc.identifier.citedreferenceGiovannoni, S. J., Thrash, J. C., & Temperton, B. ( 2014 ). Implications of streamlining theory for microbial ecology. ISME Journal, 8, 1553 – 1565. https://doi.org/10.1038/ismej.2014.60
dc.identifier.citedreferenceGiovannoni, S. J., Tripp, H. J., Givan, S., Podar, M., Vergin, K. L., Baptiasa, D., … Rappé, M. S. ( 2005 ). Genome streamlining in a cosmopolitan oceanic bacterium. Science, 309, 1242 – 1245. https://doi.org/10.1126/science.1114057
dc.identifier.citedreferenceGunawan, J., Simard, D., Gilbert, M., Lovering, A. L., Wakarchuk, W. W., Tanner, M. E., & Strynadka, N. C. J. ( 2005 ). Structural and mechanistic analysis of sialic acid synthase NeuB from Neisseria meningitidis in complex with Mn2+, phosphoenolpyruvate, and N‐acetylmannosaminitol. Journal of Biological Chemistry, 280, 3555 – 3563.
dc.identifier.citedreferenceHarke, M. J., Berry, D. L., Ammerman, J. W., & Gobler, C. J. ( 2012 ). Molecular response of the bloom‐forming cyanobacterium, Microcystis aeruginosa, to phosphorus limitation. Microbial Ecology, 63, 188 – 198. https://doi.org/10.1007/s00248-011-9894-8
dc.identifier.citedreferenceHeisler, J., Glibert, P. M., Burkholder, J. M., Anderson, D. M., Cochlan, W., Dennison, W. C., … Suddleson, M. ( 2008 ). Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae, 8, 3 – 13. https://doi.org/10.1016/j.hal.2008.08.006
dc.identifier.citedreferenceHooper, L. V., & Gordon, J. I. ( 2001 ). Glycans as legislators of host–microbial interactions: Spanning the spectrum from symbiosis to pathogenicity. Glycobiology, 11, 1 – 10. https://doi.org/10.1093/glycob/11.2.1R
dc.identifier.citedreferenceHumbert, J.‐F., Barbe, V., Latifi, A., Gugger, M., Calteau, A., Coursin, T., … de Marsac, N. T. ( 2013 ). A tribute to disorder in the genome of the bloom‐forming freshwater cyanobacterium Microcystis aeruginosa. PLoS ONE, 8, e70747. https://doi.org/10.1371/journal.pone.0070747
dc.identifier.citedreferenceHuntemann, M., Ivanova, N. N., Mavromatis, K., Tripp, H. J., Paez‐Espino, D., Palaniappan, K., … Kyrpides, N. C. ( 2015 ). The standard operating procedure of the DOE‐JGI Microbial Genome Annotation Pipeline (MGAP v.4). Standards in Genomic Sciences, 10, 86. https://doi.org/10.1186/s40793-015-0077-y
dc.identifier.citedreferenceJackrel, S. L., White, J. D., Evans, J. T., Buffin, K., Hayden, K., Sarnelle, O., & Denef, V. J. ( 2019 ). Microcystis cultures isolated from Michigan inland lakes genome sequencing, assembly, and targeted locus. NCBI SRA.
dc.identifier.citedreferenceJasti, S., Sieracki, M. E., Poulton, N. J., Giewat, M. W., & Rooney‐Varga, J. N. ( 2005 ). Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Applied and Environmental Microbiology, 71, 3483 – 3494.
dc.identifier.citedreferenceJohnson, Z. I., Zinser, E. R., Coe, A., McNulty, N. P., Woodward, E. M. S., & Chisholm, S. W. ( 2006 ). Niche partitioning among Prochlorococcus ecotypes along ocean‐scale environmental gradients. Science, 311, 1737 – 1740. https://doi.org/10.1126/science.1118052
dc.identifier.citedreferenceJoshi, N. A., & Fass, J. N. ( 2011 ). Sickle: A sliding‐window, adaptive, quality‐based trimming tool for FastQ files. v.1.33.
dc.identifier.citedreferenceKaneko, T., Nakajima, N., Okamoto, S., Suzuki, I., Tanabe, Y., Tamaoki, M., … Watanabe, M. M. ( 2007 ). Complete genomic structure of the bloom‐forming toxic cyanobacterium Microcystis aeruginosa NIES‐843. DNA Research, 14, 247 – 256. https://doi.org/10.1093/dnares/dsm026
dc.identifier.citedreferenceKathuria, S., & Martiny, A. C. ( 2011 ). Prevalence of a calcium‐based alkaline phosphatase associated with the marine cyanobacterium Prochlorococcus and other ocean bacteria. Environmental Microbiology, 13, 74 – 83.
dc.identifier.citedreferenceKessel, M., & Eloff, J. N. ( 1975 ). The ultrastructure and development of the colonial sheath of Microcystis marginata. Archives of Microbiology, 106, 209 – 214. https://doi.org/10.1007/BF00446525
dc.identifier.citedreferenceKnoll, L. B., Sarnelle, O., Hamilton, S. K., Scheele, C. E. H., Wilson, A. E., Rose, J. B., & Morgan, M. R. ( 2008 ). Invasive zebra mussels ( Dreissena polymorpha ) increase cyanobacterial toxin concentrations in low‐nutrient lakes. Canadian Journal of Fisheries and Aquatic Sciences, 65, 448 – 455.
dc.identifier.citedreferenceKoch, A. L. ( 2001 ). Oligotrophs versus copiotrophs. BioEssays, 23, 657 – 661. https://doi.org/10.1002/bies.1091
dc.identifier.citedreferenceKozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. ( 2013 ). Development of a dual‐index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Applied and Environmental Microbiology, 79, 5112 – 5120. https://doi.org/10.1128/AEM.01043-13
dc.identifier.citedreferenceLaczny, C. C., Sternal, T., Plugaru, V., Gawron, P., Atashpendar, A., Margossian, H. H., … Wilmes, P. ( 2015 ). VizBin‐an application for reference‐independent visualization and human‐augmented binning of metagenomic data. Microbiome, 3, 1. https://doi.org/10.1186/s40168-014-0066-1
dc.identifier.citedreferenceLakeman, M. B., von Dassow, P., & Cattolico, R. A. ( 2009 ). The strain concept in phytoplankton ecology. Harmful Algae, 8, 746 – 758. https://doi.org/10.1016/j.hal.2008.11.011
dc.identifier.citedreferenceLamichhaney, S., Berglund, J., Almén, M. S., Maqbool, K., Grabherr, M., Martinez‐Barrio, A., … Andersson, L. ( 2015 ). Evolution of Darwin’s finches and their beaks revealed by genome sequencing. Nature, 518, 371. https://doi.org/10.1038/nature14181
dc.identifier.citedreferenceLau, J. A., & Lennon, J. T. ( 2012 ). Rapid responses of soil microorganisms improve plant fitness in novel environments. Proceedings of the National Academy of Sciences of the United States of America, 109, 14058 – 14062. https://doi.org/10.1073/pnas.1202319109
dc.identifier.citedreferenceLi, H., & Durbin, R. ( 2009 ). Fast and accurate short read alignment with Burrows‐Wheeler transform. Bioinformatics, 25, 1754 – 1760. https://doi.org/10.1093/bioinformatics/btp324
dc.identifier.citedreferenceLi, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., … Durbin, R. ( 2009 ). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078 – 2079. https://doi.org/10.1093/bioinformatics/btp352
dc.identifier.citedreferenceLouati, I., Pascault, N., Debroas, D., Bernard, D., Humbert, J. F., & Leloup, J. ( 2015 ). Structural diversity of bacterial communities associated with bloom‐forming freshwater cyanobacteria differs according to the cyanobacterial genus. PLoS ONE, 10, e0140614. https://doi.org/10.1371/journal.pone.0140614
dc.identifier.citedreferenceLundberg, D. S., Lebeis, S. L., Herrera Paredes, S., Yourstone, S., Gehring, J., Malfatti, S., … Dangl, J. L. ( 2012 ). Defining the core Arabidopsis thaliana root microbiome. Nature, 488, 86 – 90. https://doi.org/10.1038/nature11237
dc.identifier.citedreferenceLuo, H., Benner, R., Long, R. A., & Hu, J. ( 2009 ). Subcellular localization of marine bacterial alkaline phosphatases. Proceedings of the National Academy of Sciences of the United States of America, 106, 21219 – 21223. https://doi.org/10.1073/pnas.0907586106
dc.identifier.citedreferenceMary, I., & Vaulot, D. ( 2003 ). Two-component systems in Prochlorococcus MED4: Genomic analysis and differential expression under stress. FEMS Microbiology Letters, 226, 135 – 144.
dc.identifier.citedreferenceMasango, M. G., Myrburgh, J. G., Labuschagne, L., Govender, D., Bengis, R. G., & Naicker, D. ( 2010 ). Assessment of Microcystis bloom toxicity associated with wildlife mortality in the Kruger National Park, South Africa. Journal of Wildlife Diseases, 46, 95 – 102. https://doi.org/10.7589/0090-3558-46.1.95
dc.identifier.citedreferenceMcMurdie, P. J., & Homes, S. ( 2014 ). Waste not, want not: Why rarefying microbiome data is inadmissible. PloS Computational Biology, 10, e1003531. https://doi.org/10.1371/journal.pcbi.1003531
dc.identifier.citedreferenceMenzel, D. W., & Corwin, N. ( 1965 ). The measurement of total phosphorus in seawater based on the liberation of organically bound fractions by persulfate oxidation 1. Limnology and Oceanography, 10, 280 – 282. https://doi.org/10.4319/lo.1965.10.2.0280
dc.identifier.citedreferenceMeyer, K. A., Davis, T. W., Watson, S. B., Denef, V. J., Berry, M. A., & Dick, G. J. ( 2017 ). Genome sequences of lower Great Lakes Microcystis sp. reveal strain‐specific genes that are present and expressed in western Lake Erie blooms. PLoS ONE, 12, e0183859.
dc.identifier.citedreferenceMichalak, A. M., Anderson, E. J., Beletsky, D., Boland, S., Bosch, N. S., Bridgeman, T. B., … Zagorski, M. A. ( 2013 ). Record‐setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proceedings of the National Academy of Sciences of the United States of America, 110, 6448 – 6452. https://doi.org/10.1073/pnas.1216006110
dc.identifier.citedreferenceMorris, J. J., Lenski, R. E., & Zinser, E. R. ( 2012 ). The Black Queen Hypothesis: Evolution of dependencies through adaptive gene loss. MBio, 3, e00036‐12. https://doi.org/10.1128/mBio.00036-12
dc.identifier.citedreferenceMoslavac, S., Mirus, O., Bredemeier, R., Soll, J., von Haeseler, A., & Schleiff, E. ( 2005 ). Conserved pore‐forming regions in polypeptide‐transporting proteins. The FEBS Journal, 272, 1367 – 1378. https://doi.org/10.1111/j.1742-4658.2005.04569.x
dc.identifier.citedreferenceMurphy, J., & Riley, J. P. ( 1962 ). A modified single solution method for the determination of phosphate in natural waters. Analytica Chimica Acta, 27, 31 – 36. https://doi.org/10.1016/S0003-2670(00)88444-5
dc.identifier.citedreferenceNewton, R. J., Jones, S. E., Eiler, A., McMahon, K. D., & Bertilsson, S. ( 2011 ). A guide to the natural history of freshwater lake bacteria. Microbiology and Molecular Biology Reviews, 75, 14 – 49. https://doi.org/10.1128/MMBR.00028-10
dc.identifier.citedreferenceNienaber, A., Huber, A., Göttfert, M., Hennecke, H., & Fischer, H. M. ( 2000 ). Three new NifA‐regulated genes in the Bradyrhizobium japonicum symbiotic gene region discovered by competitive DNA‐RNA hybridization. Journal of Bacteriology, 182, 1472 – 1480. https://doi.org/10.1128/JB.182.6.1472-1480.2000
dc.identifier.citedreferenceOlm, M. R., Brown, C. T., Brooks, B., & Banfield, J. F. ( 2017 ). dRep: A tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de‐replication. ISME Journal, 11, 2864 – 2868. https://doi.org/10.1038/ismej.2017.126
dc.identifier.citedreferenceParks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P., & Tyson, G. W. ( 2015 ). CheckM: Assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Research, 25, 1 – 13. https://doi.org/10.1101/gr.186072.114
dc.identifier.citedreferenceParks, D. H., Tyson, G. W., Hugenholtz, P., & Beiko, R. G. ( 2014 ). STAMP: Statistical analysis of taxonomic and functional profiles. Bioinformatics, 30, 3123 – 3124. https://doi.org/10.1093/bioinformatics/btu494
dc.identifier.citedreferencePeiffer, J. A., Spor, A., Koren, O., Jin, Z., Green Tringe, S., Dangl, J. L., … Ley, R. E. ( 2013 ). Diversity and heritability of the maize rhizosphere microbiome under field conditions. Proceedings of the National Academy of Sciences of the United States of America, 110, 6548 – 6553. https://doi.org/10.1073/pnas.1302837110
dc.identifier.citedreferencePfennig, D. W., Wund, M. A., Snell‐Rood, E. C., Cruickshank, T., Schlichting, C. D., & Moczek, A. P. ( 2010 ). Phenotypic plasticity impacts on diversification and speciation. Trends in Ecology & Evolution, 25, 459 – 467.
dc.identifier.citedreferencePlude, J. L., Parker, D. L., Schommer, O. J., Timmerman, R. J., Hagstrom, S. A., Joers, J. M., & Hnasko, R. ( 1991 ). Chemical characterization of polysaccharide from the slime layer of the cyanobacterium Microcystis flos‐aquae C3–40. Applied and Environmental Microbiology, 57, 1696 – 1700.
dc.identifier.citedreferencePost, D. M., Palkovacs, E. P., Schielke, E. G., & Dodson, S. I. ( 2008 ). Intraspecific variation in a predator affects community structure and cascading trophic interactions. Ecology, 89, 2019 – 2032. https://doi.org/10.1890/07-1216.1
dc.identifier.citedreferencePritchard, L., Glover, R. H., Humphris, S., Elphinstone, J. G., & Toth, I. K. ( 2016 ). Genomics and taxonomy in diagnostics for food security: Soft‐rotting enterobacterial plant pathogens. Analytical Methods, 8, 12 – 24. https://doi.org/10.1039/C5AY02550H
dc.identifier.citedreferenceQin, B., Zhu, G., Gao, G., Zhang, Y., Li, W., Paerl, H. W., & Carmichael, W. W. ( 2010 ). A drinking water crisis in Lake Taihu, China: Linkage to climatic variability and lake management. Environmental Management, 45, 105 – 112. https://doi.org/10.1007/s00267-009-9393-6
dc.identifier.citedreferenceQuast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., … Glöckner, F. O. ( 2012 ). The SILVA ribosomal RNA gene database project: Improved data processing and web‐based tools. Nucleic Acids Research, 41, D590 – D596. https://doi.org/10.1093/nar/gks1219
dc.identifier.citedreferenceRaikow, D. F., Sarnelle, O., Wilson, A. E., & Hamilton, S. K. ( 2004 ). Dominance of the noxious cyanobacterium Microcystis aeruginosa in low‐nutrient lakes is associated with exotic zebra mussels. Limnology and Oceanography, 49, 482 – 487.
dc.identifier.citedreferenceRambaut, A. ( 2012 ). FigTree v1. 4. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/. Accessed December 12, 2018.
dc.identifier.citedreferenceReynolds, C. S. ( 2006 ). The ecology of phytoplankton. Cambridge, UK: Cambridge University Press.
dc.identifier.citedreferenceRichter, M., & Rosselló‐Móra, R. ( 2009 ). Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106, 19126 – 19131. https://doi.org/10.1073/pnas.0906412106
dc.identifier.citedreferenceRocap, G., Larimer, F. W., Lamerdin, J., Malfatti, S., Chain, P., Ahlgren, N. A., … Chisholm, S. W. ( 2003 ). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature, 424, 1042 – 1047. https://doi.org/10.1038/nature01947
dc.identifier.citedreferenceRodrigues, M., Ostermann, T., Kremeser, L., Lindner, H., Beisel, C., Berezikov, E., … Ladurner, P. ( 2016 ). Profiling of adhesive-related genes in the freshwater cndiarian Hydra magnipapillata by transcriptomics and proteomics. Biofouling, 32, 1115 – 1129.
dc.identifier.citedreferenceRohrlack, T., Henning, M., & Kohl, J. G. ( 1999 ). Mechanisms of the inhibitory effect of the cyanobacterium Microcystis aeruginosa on Daphnia galeata ’s ingestion rate. Journal of Plankton Research, 21, 1489 – 1500. https://doi.org/10.1093/plankt/21.8.1489
dc.identifier.citedreferenceSahm, A., Berns, M., Platzer, M., & Szafranski, K. ( 2017 ). PosiGene: Automated and easy‐to‐use pipeline for genome‐wide detection of positively selected genes. Nucleic Acids Research, 45, 1 – 11. https://doi.org/10.1093/nar/gkx179
dc.identifier.citedreferenceSarnelle, O., Morrison, J., Kaul, R., Horst, G., Wandell, H., & Bednarz, R. ( 2010 ). Citizen monitoring: Testing hypotheses about the interactive influences of eutrophication and mussel invasion on a cyanobacterial toxin in lakes. Water Research, 44, 141 – 150. https://doi.org/10.1016/j.watres.2009.09.014
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.