Neutral Evolution and Dispersal Limitation Produce Biogeographic Patterns in Microcystis aeruginosa Populations of Lake Systems

Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dis...

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Published inMicrobial ecology Vol. 74; no. 2; pp. 416 - 426
Main Authors Shirani, Sahar, Hellweger, Ferdi L.
Format Journal Article
LanguageEnglish
Published New York Springer Science + Business Media 01.08.2017
Springer US
Springer Nature B.V
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ISSN0095-3628
1432-184X
1432-184X
DOI10.1007/s00248-017-0963-5

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Abstract Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.
AbstractList Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.
Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.
Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.
Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role of environmental selection and neutral processes in the biogeography of these systems. Here, we quantify the effect of genetic drift and dispersal limitation by simulating individual cyanobacteria cells using an agent-based model (ABM). In the model, cells grow (divide), die, and migrate between lakes. Each cell has a full genome that is subject to neutral mutation (i.e., the growth rate is independent of the genome). The model is verified by simulating simplified lake systems, for which theoretical solutions are available. Then, it is used to simulate the biogeography of the cyanobacterium Microcystis aeruginosa in a number of real systems, including the Great Lakes, Klamath River, Yahara River, and Chattahoochee River. Model output is analyzed using standard bioinformatics tools (BLAST, MAFFT). The emergent patterns of nucleotide divergence between lakes are dynamic, including gradual increases due to accumulation of mutations and abrupt changes due to population takeovers by migrant cells (coalescence events). The model predicted nucleotide divergence is heterogeneous within systems, and for weakly connected lakes, it can be substantial. For example, Lakes Superior and Michigan are predicted to have an average genomic nucleotide divergence of 8200 bp or 0.14%. The divergence between more strongly connected lakes is much lower. Our results provide a quantitative baseline for future biogeography studies. They show that dispersal limitation can be an important factor in microbe biogeography, which is contrary to the common belief, and could affect how a system responds to environmental change.
Author Shirani, Sahar
Hellweger, Ferdi L.
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Keywords Biogeography
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Neutral evolution
Lake systems
Cyanobacteria
Dispersal limitation
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References_xml – reference: OttenTGCrosswellJRMackeySDreherTWApplication of molecular tools for microbial source tracking and public health risk assessment of a Microcystis bloom traversing 300km of the Klamath RiverHarmful Algae201546718110.1016/j.hal.2015.05.007
– reference: KashtanNRoggensackSERodrigueSThompsonJWBillerSJCoeADingHMarttinenPMalmstromRRStockerRFollowsMJStepanauskasRChisholmSWSingle-cell genomics reveals hundreds of coexisting subpopulations in wild ProchlorococcusScience201434461824164201:CAS:528:DC%2BC2cXmsFWmtLo%3D10.1126/science.124857524763590
– reference: StrobeckCAverage number of nucleotide differences in a sample from a single subpopulation: a test for population subdivisionGenetics198711711491531:STN:280:DC%2BC3crpt1SmsQ%3D%3D172463961203183
– reference: LindströmESForslundMAlgestenGBergströmAKExternal control of bacterial community structure in lakesLimnol. Oceanogr.200651133934210.4319/lo.2006.51.1.0339
– reference: CostasEFlores-MoyaALópez-RodasVRapid adaptation of phytoplankters to geothermal waters is achieved by single mutations: were extreme environments ‘Noah's arks’ for photosynthesizers during the Neoproterozoic ‘snowball earth’?New Phytol.2008180492293210.1111/j.1469-8137.2008.02620.x18803596
– reference: KreftJ-UPluggeCMGrimmVPratsCLeveauJHJBanitzTBainesSClarkJRosAKlapperIToppingCJFieldAJSchulerALitchmanEHellwegerFLMighty small: observing and modeling individual microbes becomes big scienceProc. Natl. Acad. Sci.20131104518027180281:CAS:528:DC%2BC3sXhvVSmurzM10.1073/pnas.1317472110241945303831448
– reference: KristiansenJ16. Dispersal of freshwater algae — a reviewHydrobiologia1996336115115710.1007/BF00010829
– reference: WrightSIsolation by distanceGenetics19432821141:STN:280:DC%2BD2s%2FmsFSmsg%3D%3D172470741209196
– reference: Hamilton M (2011) Population genetics. John Wiley & Sons
– reference: HaydenCJBemanJMMicrobial diversity and community structure along a lake elevation gradient in Yosemite National Park, CaliforniaUSA. Environmental Microbiology201526058326
– reference: del MarF-AMBañares-EspañaEGarcía-SánchezMJHernández-LópezMLópez-RodasVCostasEFlores-MoyaADisentangling mechanisms involved in the adaptation of photosynthetic microorganisms to the extreme Sulphureous water from los Baños de Vilo (S Spain)Microb. Ecol.201366474275110.1007/s00248-013-0268-2
– reference: ConditRPitmanNLeighEGChaveJTerborghJFosterRBNúñezPAguilarSValenciaRVillaGMuller-LandauHCLososEHubbellSPBeta-diversity in tropical Forest treesScience200229555556666691:CAS:528:DC%2BD38XptF2ntg%3D%3D10.1126/science.106685411809969
– reference: HellwegerFLvan SebilleEFredrickNDBiogeographic patterns in ocean microbes emerge in a neutral agent-based modelScience20143456202134613491:CAS:528:DC%2BC2cXhsV2qtL%2FF10.1126/science.125442125214628
– reference: Zwirglmaier K, Keiz K, Engel M, Geist J, Raeder U (2015) Seasonal and spatial patterns of microbial diversity along a trophic gradient in the interconnected lakes of the Osterseen Lake District, Bavaria. Front. Microbiol. 6
– reference: RaghavanRKelkarYDOchmanHA selective force favoring increased G+C content in bacterial genesProc. Natl. Acad. Sci.20121093614504145071:CAS:528:DC%2BC38XhsVaqu77L10.1073/pnas.1205683109229082963437849
– reference: LongHMillerSFStraussCZhaoCChengLYeZGriffinKTeRLeeHChenC-CLynchMAntibiotic treatment enhances the genome-wide mutation rate of target cellsProc. Natl. Acad. Sci.201611318E2498E25051:CAS:528:DC%2BC28Xmt1Shtbo%3D10.1073/pnas.1601208113270919914983809
– reference: RecheIPulido-VillenaEMorales-BaqueroRCasamayorEODoes ecosystem size determine aquatic bacterial richness?Ecology20058671715172210.1890/04-1587
– reference: Van der GuchtKCottenieKMuylaertKVloemansNCousinSDeclerckSJeppesenEConde-PorcunaJMSchwenkKZwartGDegansHVyvermanWDe MeesterLThe power of species sorting: local factors drive bacterial community composition over a wide range of spatial scalesProc. Natl. Acad. Sci. U. S. A.20071045120404204091:CAS:528:DC%2BD1cXjslenuw%3D%3D10.1073/pnas.0707200104180773712154443
– reference: DavisTWWatsonSBRozmarynowyczMJCiborowskiJJHMcKayRMBullerjahnGSPhylogenies of microcystin-producing cyanobacteria in the lower Laurentian Great Lakes suggest extensive genetic connectivityPLoS One201499e10609310.1371/journal.pone.0106093252079414160157
– reference: ChapraSCDolanDMGreat Lakes total phosphorus revisited: 2. Mass balance modelingJ. Great Lakes Res.20123847417541:CAS:528:DC%2BC38XhslSltbfP10.1016/j.jglr.2012.10.002
– reference: TanabeYKasaiFWatanabeMMMultilocus sequence typing (MLST) reveals high genetic diversity and clonal population structure of the toxic cyanobacterium Microcystis aeruginosaMicrobiology200715311369537031:CAS:528:DC%2BD2sXhtlGmsbjM10.1099/mic.0.2007/010645-017975077
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– reference: MillerTRMcMahonKDGenetic diversity of cyanobacteria in four eutrophic lakesFEMS Microbiol. Ecol.20117823363481:CAS:528:DC%2BC3MXhsVCksrnN10.1111/j.1574-6941.2011.01162.x21707672
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– reference: ReavieEDBarbieroRPAllingerLEWarrenGJPhytoplankton trends in the Great Lakes, 2001–2011J. Great Lakes Res.201440361863910.1016/j.jglr.2014.04.013%@ 0380-1330
– reference: ReynoldsCSIrishAEModelling phytoplankton dynamics in lakes and reservoirs: the problem of in-situ growth ratesHydrobiologia19973491–35171:CAS:528:DyaK2sXnslOit7g%3D10.1023/A:1003020823129
– reference: López-RodasVFlores-MoyaAManeiroEPerdigonesNMarvaFGarcíaMECostasEResistance to glyphosate in the cyanobacterium Microcystis aeruginosa as result of pre-selective mutationsEvol. Ecol.200721453554710.1007/s10682-006-9134-8
– reference: BeversdorfLJMillerTRMcMahonKDThe role of nitrogen fixation in cyanobacterial bloom toxicity in a temperate, eutrophic lakePLoS One201382e561031:CAS:528:DC%2BC3sXivFKjsbk%3D10.1371/journal.pone.0056103234052553566065
– reference: LynchMAckermanMSGoutJ-FLongHSungWThomasWKFosterPLGenetic drift, selection and the evolution of the mutation rateNat Rev Genet201617117047141:CAS:528:DC%2BC28Xhs1yitLzP10.1038/nrg.2016.10427739533http://www.nature.com/nrg/journal/v17/n11/abs/nrg.2016.104.html#supplementary-information
– reference: KutovayaOAMcKayRMLBeallBFNWilhelmSWKaneDDChaffinJDBridgemanTBBullerjahnGSEvidence against fluvial seeding of recurrent toxic blooms of Microcystis spp. in Lake Erie’s western basinHarmful Algae201215717710.1016/j.hal.2011.11.007
– reference: MillerTRBeversdorfLChastonSDMcMahonKDSpatiotemporal molecular analysis of cyanobacteria blooms reveals Microcystis-Aphanizomenon interactionsPLoS One201389e749331:CAS:528:DC%2BC3sXhsFOntLfN10.1371/journal.pone.0074933240864003785500
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– reference: FuhrmanJASchwalbachMSStinglUProteorhodopsins: an array of physiological roles?Nat Rev Micro2008664884941:CAS:528:DC%2BD1cXlvFSisbw%3D
– reference: Garcίa-VilladaLRicoMAltamiranoMSánchezmartίnLLópez-RodasVCostasEOccurrence of copper resistant mutants in the toxic cyanobacteria Microcystis aeruginosa: characterisation and future implications in the use of copper sulphate as algaecideWater Res.20043882207221310.1016/j.watres.2004.01.036
– reference: Moore D, Badzinski S, Cuthbert F, Wires L (2016) Waterbird & waterfowl monitoring on the Canadian Great Lakes. http://glc.org/files/2016-Waterbird-Canadian-Studies.pdf. Accessed 9/9/2016 2016
– reference: DybleJFahnenstielGLLitakerRWMillieDFTesterPAMicrocystin concentrations and genetic diversity of Microcystis in the lower Great LakesEnviron. Toxicol.20082345075161:CAS:528:DC%2BD1cXovFWntrc%3D10.1002/tox.2037018247416
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Snippet Molecular observations reveal substantial biogeographic patterns of cyanobacteria within systems of connected lakes. An important question is the relative role...
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SubjectTerms Accumulation
Biogeography
Bioinformatics
Biomedical and Life Sciences
Cell migration
Cells
Coalescence
Coalescing
Computer simulation
Cyanobacteria
Dispersal
Dispersion
Divergence
Dynamical systems
Ecology
Environmental changes
ENVIRONMENTAL MICROBIOLOGY
evolution
Evolution, Molecular
Genetic Drift
genome
Genomes
Geoecology/Natural Processes
Great Lakes
Great Lakes Region
Growth rate
Lakes
Lakes - microbiology
Life Sciences
Mathematical models
Michigan
Microbial Ecology
Microbiology
Microcystis
Microcystis - genetics
Microcystis aeruginosa
Mutation
Nature Conservation
Nucleotides
Populations
Rivers
Solutions
Water Quality/Water Pollution
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Title Neutral Evolution and Dispersal Limitation Produce Biogeographic Patterns in Microcystis aeruginosa Populations of Lake Systems
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