Origin of biogeographically distinct ecotypes during laboratory evolution.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
28 Aug 2024
28 Aug 2024
Historique:
received:
05
06
2023
accepted:
15
08
2024
medline:
31
8
2024
pubmed:
31
8
2024
entrez:
28
8
2024
Statut:
epublish
Résumé
Resource partitioning is central to the incredible productivity of microbial communities, including gigatons in annual methane emissions through syntrophic interactions. Previous work revealed how a sulfate reducer (Desulfovibrio vulgaris, Dv) and a methanogen (Methanococcus maripaludis, Mm) underwent evolutionary diversification in a planktonic context, improving stability, cooperativity, and productivity within 300-1000 generations. Here, we show that mutations in just 15 Dv and 7 Mm genes within a minimal assemblage of this evolved community gave rise to co-existing ecotypes that were spatially enriched within a few days of culturing in a fluidized bed reactor. The spatially segregated communities partitioned resources in the simulated subsurface environment, with greater lactate utilization by attached Dv but partial utilization of resulting H
Identifiants
pubmed: 39198408
doi: 10.1038/s41467-024-51759-y
pii: 10.1038/s41467-024-51759-y
doi:
Substances chimiques
Methane
OP0UW79H66
Hydrogen
7YNJ3PO35Z
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7451Subventions
Organisme : DOE | Office of Science (SC)
ID : DE-AC02-05CH11231
Informations de copyright
© 2024. The Author(s).
Références
Flemming, H.-C. & Wuertz, S. Bacteria and archaea on Earth and their abundance in biofilms. Nat. Rev. Microbiol. 17, 247–260 (2019).
pubmed: 30760902
doi: 10.1038/s41579-019-0158-9
Hunt, D. E. et al. Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton. Science 320, 1081–1085 (2008).
pubmed: 18497299
doi: 10.1126/science.1157890
Johnson, Z. I. et al. Niche Partitioning Among Prochlorococcus Ecotypes Along Ocean-Scale Environmental Gradients. Science 311, 1737–1740 (2006).
pubmed: 16556835
doi: 10.1126/science.1118052
Smith, H. J. et al. Impact of hydrologic boundaries on microbial planktonic and biofilm communities in shallow terrestrial subsurface environments. Fems Microbiol. Ecol. 94, fiy191 (2018).
pubmed: 30265315
pmcid: 6192502
doi: 10.1093/femsec/fiy191
Clark, M. E. et al. Transcriptomic and proteomic analyses of Desulfovibrio vulgaris biofilms: Carbon and energy flow contribute to the distinct biofilm growth state. Bmc Genomics 13, 138–138 (2012).
pubmed: 22507456
pmcid: 3431258
doi: 10.1186/1471-2164-13-138
Kurczy, M. E. et al. Comprehensive bioimaging with fluorinated nanoparticles using breathable liquids. Nat. Commun. 6, 5998 (2015).
pubmed: 25601659
doi: 10.1038/ncomms6998
Stylo, M., Neubert, N., Roebbert, Y., Weyer, S. & Bernier-Latmani, R. Mechanism of Uranium Reduction and Immobilization in Desulfovibrio vulgaris Biofilms. Environ. Sci. Technol. 49, 10553–10561 (2015).
pubmed: 26251962
doi: 10.1021/acs.est.5b01769
Hansen, S. K., Rainey, P. B., Haagensen, J. A. J. & Molin, S. Evolution of species interactions in a biofilm community. Nature 445, 533–536 (2007).
pubmed: 17268468
doi: 10.1038/nature05514
Friesen, M. L., Saxer, G., Travisano, M. & Doebeli, M. Experimental evidence for sympatric ecological diversification due to frequency-dependent competition in escherichia coli. Evolution 58, 245–260 (2004).
pubmed: 15068343
Friedman, J., Alm, E. J. & Shapiro, B. J. Sympatric Speciation: When Is It Possible in Bacteria? Plos One 8, e53539 (2013).
pubmed: 23349716
pmcid: 3547939
doi: 10.1371/journal.pone.0053539
Lassalle, F., Muller, D. & Nesme, X. Ecological speciation in bacteria: reverse ecology approaches reveal the adaptive part of bacterial cladogenesis. Res. Microbiol. 166, 729–741 (2015).
pubmed: 26192210
doi: 10.1016/j.resmic.2015.06.008
Thauer, R. K. Anaerobic oxidation of methane with sulfate: on the reversibility of the reactions that are catalyzed by enzymes also involved in methanogenesis from CO
pubmed: 21489863
doi: 10.1016/j.mib.2011.03.003
Stams, A. J. M. & Plugge, C. M. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat. Rev. Microbiol. 7, 568–577 (2009).
pubmed: 19609258
doi: 10.1038/nrmicro2166
Plugge, C. M., Zhang, W., Scholten, J. C. M. & Stams, A. J. M. Metabolic Flexibility of Sulfate-Reducing Bacteria. Front. Microbiol. 2, 81 (2011).
pubmed: 21734907
pmcid: 3119409
doi: 10.3389/fmicb.2011.00081
Brileya, K. A., Camilleri, L. B., Zane, G. M., Wall, J. D. & Fields, M. W. Biofilm growth mode promotes maximum carrying capacity and community stability during product inhibition syntrophy. Front Microbiol 5, 693 (2014).
pubmed: 25566209
pmcid: 4266047
doi: 10.3389/fmicb.2014.00693
Walker, C. B. et al. Functional responses of methanogenic archaea to syntrophic growth. Isme J. 6, 2045–2055 (2012).
pubmed: 22739494
pmcid: 3475374
doi: 10.1038/ismej.2012.60
Stolyar, S. et al. Metabolic modeling of a mutualistic microbial community. Mol. Syst. Biol. 3, 92–92 (2007).
pubmed: 17353934
pmcid: 1847946
doi: 10.1038/msb4100131
Walker, C. B. et al. The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J. Bacteriol. 191, 5793–5801 (2009).
pubmed: 19581361
pmcid: 2737945
doi: 10.1128/JB.00356-09
Heidelberg, J. F. et al. The genome sequence of the anaerobic, sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol. 22, 554–559 (2004).
pubmed: 15077118
doi: 10.1038/nbt959
Hendrickson, E. L. et al. Complete Genome Sequence of the Genetically Tractable Hydrogenotrophic Methanogen Methanococcus maripaludis. J. Bacteriol. 186, 6956–6969 (2004).
pubmed: 15466049
pmcid: 522202
doi: 10.1128/JB.186.20.6956-6969.2004
Turkarslan, S. et al. Mechanism for microbial population collapse in a fluctuating resource environment. Mol. Syst. Biol. 13, 919 (2017).
pubmed: 28320772
pmcid: 5371734
doi: 10.15252/msb.20167058
Turkarslan, S. et al. Synergistic epistasis enhances the co-operativity of mutualistic interspecies interactions. Isme J. 15, 2233–2247 (2021).
pubmed: 33612833
pmcid: 8319347
doi: 10.1038/s41396-021-00919-9
Hillesland, K. L. et al. Erosion of functional independence early in the evolution of a microbial mutualism. Proc. Natl Acad. Sci. 111, 14822–14827 (2014).
pubmed: 25267659
pmcid: 4205623
doi: 10.1073/pnas.1407986111
Hillesland, K. L. & Stahl, D. A. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl Acad. Sci. 107, 2124–2129 (2010).
pubmed: 20133857
pmcid: 2836651
doi: 10.1073/pnas.0908456107
Thompson, A. W. et al. Robustness of a model microbial community emerges from population structure among single cells of a clonal population. Environ. Microbiol. 19, 3059–3069 (2017).
pubmed: 28419704
doi: 10.1111/1462-2920.13764
McInerney, M. J., Sieber, J. R. & Gunsalus, R. P. Syntrophy in anaerobic global carbon cycles. Curr. Opin. Biotech. 20, 623–632 (2009).
pubmed: 19897353
doi: 10.1016/j.copbio.2009.10.001
Meyer, B. et al. Variation among Desulfovibrio Species in Electron Transfer Systems Used for Syntrophic Growth. J. Bacteriol. 195, 990–1004 (2012).
pubmed: 23264581
doi: 10.1128/JB.01959-12
Moore, B. C. & Leigh, J. A. Markerless Mutagenesis in Methanococcus maripaludis Demonstrates Roles for Alanine Dehydrogenase, Alanine Racemase, and Alanine Permease. J. Bacteriol. 187, 972–979 (2005).
pubmed: 15659675
pmcid: 545699
doi: 10.1128/JB.187.3.972-979.2005
Papkou, A., Hedge, J., Kapel, N., Young, B. & MacLean, R. C. Efflux pump activity potentiates the evolution of antibiotic resistance across S. aureus isolates. Nat. Commun. 11, 3970 (2020).
pubmed: 32769975
pmcid: 7414891
doi: 10.1038/s41467-020-17735-y
Markert, J. A. et al. Population genetic diversity and fitness in multiple environments. Bmc Evol. Biol. 10, 205 (2010).
pubmed: 20609254
pmcid: 2927917
doi: 10.1186/1471-2148-10-205
Langwaldt, J. H. & Puhakka, J. A. On-site biological remediation of contaminated groundwater: a review. Environ. Pollut. 107, 187–197 (2000).
pubmed: 15092995
doi: 10.1016/S0269-7491(99)00137-2
Hwang, C. et al. Changes in bacterial community structure correlate with initial operating conditions of a field-scale denitrifying fluidized bed reactor. Appl. Microbiol. Biotechnol. 71, 748–760 (2006).
pubmed: 16292532
doi: 10.1007/s00253-005-0189-1
Colman, D. R. et al. Ecological differentiation in planktonic and sediment-associated chemotrophic microbial populations in Yellowstone hot springs. Fems Microbiol. Ecol. 92, fiw137 (2016).
pubmed: 27306555
doi: 10.1093/femsec/fiw137
Ding, Y. et al. Identification of the first transcriptional activator of an archaellum operon in a euryarchaeon. Mol. Microbiol 102, 54–70 (2016).
pubmed: 27314758
doi: 10.1111/mmi.13444
Stewart, P. S. & Franklin, M. J. Physiological heterogeneity in biofilms. Nat. Rev. Microbiol 6, 199–210 (2008).
pubmed: 18264116
doi: 10.1038/nrmicro1838
Davey, M. E. & O’toole, G. A. Microbial Biofilms: from Ecology to Molecular Genetics. Microbiol Mol. Biol. R. 64, 847–867 (2000).
doi: 10.1128/MMBR.64.4.847-867.2000
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff. Fly 6, 80–92 (2012).
pubmed: 22728672
pmcid: 3679285
doi: 10.4161/fly.19695
Wu, Z. et al. Insights into the planktonic to sessile transition in a marine biofilm-forming Pseudoalteromonas isolate using comparative proteomic analysis. Aquat. Micro. Ecol. 86, 69–84 (2021).
doi: 10.3354/ame01959
Nesper, J. et al. Characterization of Vibrio cholerae O1 El Tor galU and galE Mutants: Influence on Lipopolysaccharide Structure, Colonization, and Biofilm Formation. Infect. Immun. 69, 435–445 (2001).
pubmed: 11119535
pmcid: 97901
doi: 10.1128/IAI.69.1.435-445.2001
Guo, Y., Sagaram, U. S., Kim, J. & Wang, N. Requirement of the galU Gene for Polysaccharide Production by and Pathogenicity and Growth In Planta of Xanthomonas citri subsp. citri. Appl. Environ. Micro. 76, 2234–2242 (2010).
doi: 10.1128/AEM.02897-09
Krumholz, L. R. et al. Syntrophic Growth of Desulfovibrio alaskensis Requires Genes for H 2 and Formate Metabolism as Well as Those for Flagellum and Biofilm Formation. Appl. Environ. Micro. 81, 2339–2348 (2015).
doi: 10.1128/AEM.03358-14
Shimoyama, T., Kato, S., Ishii, S. & Watanabe, K. Flagellum Mediates Symbiosis. Science 323, 1574–1574 (2009).
pubmed: 19299611
doi: 10.1126/science.1170086
Vita, N. et al. The primary pathway for lactate oxidation in Desulfovibrio vulgaris. Front. Microbiol. 6, 606 (2015).
pubmed: 26167158
pmcid: 4481167
doi: 10.3389/fmicb.2015.00606
Clark, M. E. et al. Temporal Transcriptomic Analysis as Desulfovibrio vulgaris Hildenborough Transitions into Stationary Phase during Electron Donor Depletion. Appl. Environ. Micro. 72, 5578–5588 (2006).
doi: 10.1128/AEM.00284-06
Xia, Q. et al. Quantitative proteomics of nutrient limitation in the hydrogenotrophic methanogen Methanococcus maripaludis. Bmc Microbiol. 9, 149 (2009).
pubmed: 19627604
pmcid: 2723118
doi: 10.1186/1471-2180-9-149
Flowers, J. J., Richards, M. A., Baliga, N., Meyer, B. & Stahl, D. A. Constraint-based modelling captures the metabolic versatility of Desulfovibrio vulgaris. Env Microbiol. Rep. 10, 190–201 (2018).
doi: 10.1111/1758-2229.12619
Richards, M. A. et al. Exploring Hydrogenotrophic Methanogenesis: a Genome Scale Metabolic Reconstruction of Methanococcus maripaludis. J. Bacteriol. 198, 3379–3390 (2016).
pubmed: 27736793
pmcid: 5116941
doi: 10.1128/JB.00571-16
Becker, S. A. & Palsson, B. O. Context-Specific Metabolic Networks Are Consistent with Experiments. Plos Comput. Biol. 4, e1000082 (2008).
pubmed: 18483554
pmcid: 2366062
doi: 10.1371/journal.pcbi.1000082
Wu, Y. et al. Soil biofilm formation enhances microbial community diversity and metabolic activity. Environ. Int 132, 105116 (2019).
pubmed: 31479959
doi: 10.1016/j.envint.2019.105116
Fomina, M. & Skorochod, I. Microbial Interaction with Clay Minerals and Its Environmental and Biotechnological Implications. Miner.-basel 10, 861 (2020).
Sivadon, P., Barnier, C., Urios, L. & Grimaud, R. Biofilm formation as a microbial strategy to assimilate particulate substrates. Env Microbiol Rep. 11, 749–764 (2019).
Stewart, P. S. Diffusion in Biofilms. J. Bacteriol. 185, 1485–1491 (2003).
pubmed: 12591863
pmcid: 148055
doi: 10.1128/JB.185.5.1485-1491.2003
Stoodley, P., deBeer, D. & Lewandowski, Z. Liquid Flow in Biofilm Systems. Appl Environ. Micro. 60, 2711–2716 (1994).
doi: 10.1128/aem.60.8.2711-2716.1994
Beer, D., de, Stoodley, P. & Lewandowski, Z. Measurement of local diffusion coefficients in biofilms by microinjection and confocal microscopy. Biotechnol. Bioeng. 53, 151–158 (1997).
pubmed: 18633959
doi: 10.1002/(SICI)1097-0290(19970120)53:2<151::AID-BIT4>3.0.CO;2-N
Gorter, F. A., Manhart, M. & Ackermann, M. Understanding the evolution of interspecies interactions in microbial communities. Philos. Trans. R. Soc. B 375, 20190256 (2020).
doi: 10.1098/rstb.2019.0256
Diener, C., Gibbons, S. M. & Resendis-Antonio, O. MICOM: Metagenome-Scale Modeling To Infer Metabolic Interactions in the Gut Microbiota. mSystems 5, e00606–e00619 (2020).
pubmed: 31964767
pmcid: 6977071
doi: 10.1128/msystems.00606-19
Friedman, J., Twyford, A. D., Willis, J. H. & Blackman, B. K. The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus. Mol. Ecol. 24, 111–122 (2015).
pubmed: 25403267
doi: 10.1111/mec.13004
Bendall, M. L. et al. Genome-wide selective sweeps and gene-specific sweeps in natural bacterial populations. Isme J. 10, 1589–1601 (2016).
pubmed: 26744812
pmcid: 4918448
doi: 10.1038/ismej.2015.241
Shapiro, B. J. et al. Population Genomics of Early Events in the Ecological Differentiation of Bacteria. Science 336, 48–51 (2012).
pubmed: 22491847
pmcid: 3337212
doi: 10.1126/science.1218198
Hunt, K. A., Netzer, F., Gorman-Lewis, D. & Stahl, D. A. Microbial maintenance energy quantified and modeled with microcalorimetry. Biotechnol. Bioeng. 119, 2413–2422 (2022).
pubmed: 35680566
doi: 10.1002/bit.28155
Ewels, P., Magnusson, M., Lundin, S. & Käller, M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics 32, 3047–3048 (2016).
pubmed: 27312411
pmcid: 5039924
doi: 10.1093/bioinformatics/btw354
Turkarslan, S. Origin of biogeographically distinct ecotypes during laboratory evolution. GitHub:evolution-of.-syntrophy https://doi.org/10.5281/zenodo.12124987 (2024).
doi: 10.5281/zenodo.12124987
Krueger, F. Trim Galore: a wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Bisufite-Seq) libraries. (2012).
McKenna, A. et al. The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 20, 1297–1303 (2010).
pubmed: 20644199
pmcid: 2928508
doi: 10.1101/gr.107524.110
Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).
pubmed: 19451168
pmcid: 2705234
doi: 10.1093/bioinformatics/btp324
Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
pubmed: 19505943
pmcid: 2723002
doi: 10.1093/bioinformatics/btp352
Koboldt, D. C. et al. VarScan 2: Somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res. 22, 568–576 (2012).
pubmed: 22300766
pmcid: 3290792
doi: 10.1101/gr.129684.111
Tenaillon, O. et al. Tempo and mode of genome evolution in a 50,000-generation experiment. Nature 536, 165–170 (2016).
pubmed: 27479321
pmcid: 4988878
doi: 10.1038/nature18959
Petzoldt, T. Estimation of Growth Rates with Package Growthrates. https://cran.r-project.org/web/packages/growthrates/vignettes/User_models.html (2022).
Bray, N. L., Pimentel, H., Melsted, P. & Pachter, L. Near-optimal probabilistic RNA-seq quantification. Nat. Biotechnol. 34, 525–527 (2016).
pubmed: 27043002
doi: 10.1038/nbt.3519
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Meyer, B., Kuehl, J. V., Deutschbauer, A. M., Arkin, A. P. & Stahl, D. A. Flexibility of Syntrophic Enzyme Systems in Desulfovibrio Species Ensures Their Adaptation Capability to Environmental Changes. J. Bacteriol. 195, 4900–4914 (2013).
pubmed: 23974031
pmcid: 3807489
doi: 10.1128/JB.00504-13
Venceslau, S. S., Stockdreher, Y., Dahl, C. & Pereira, I. A. C. The “bacterial heterodisulfide” DsrC is a key protein in dissimilatory sulfur metabolism. Biochimica Et. Biophysica Acta Bba - Bioenerg. 1837, 1148–1164 (2014).
doi: 10.1016/j.bbabio.2014.03.007
Immanuel, S. R. C. Origin of biogeographically distinct ecotypes during laboratory evolution. GitHub:Metabolic model Syntrophy https://doi.org/10.5281/zenodo.12119526 (2024).
doi: 10.5281/zenodo.12119526
Schellenberger, J. et al. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0. Nat. Protoc. 6, 1290–1307 (2011).
pubmed: 21886097
pmcid: 3319681
doi: 10.1038/nprot.2011.308
Heirendt, L. et al. Creation and analysis of biochemical constraint-based models using the COBRA Toolbox v.3.0. Nat. Protoc. 14, 639–702 (2019).
pubmed: 30787451
pmcid: 6635304
doi: 10.1038/s41596-018-0098-2
Valenzuela, J. Origin of biogeographically distinct ecotypes during laboratory evolution. GitHub:Origin-of.-biogeographically-distinct.-ecotypes https://doi.org/10.5281/zenodo.12116362 (2024).
doi: 10.5281/zenodo.12116362