High genomic differentiation and limited gene flow indicate recent cryptic speciation within the genus Laspinema (cyanobacteria)

. 2022 ; 13 () : 977454. [epub] 20220909

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36160208

The sympatric occurrence of closely related lineages displaying conserved morphological and ecological traits is often characteristic of free-living microbes. Gene flow, recombination, selection, and mutations govern the genetic variability between these cryptic lineages and drive their differentiation. However, sequencing conservative molecular markers (e.g., 16S rRNA) coupled with insufficient population-level sampling hindered the study of intra-species genetic diversity and speciation in cyanobacteria. We used phylogenomics and a population genomic approach to investigate the extent of local genomic diversity and the mechanisms underlying sympatric speciation of Laspinema thermale. We found two cryptic lineages of Laspinema. The lineages were highly genetically diverse, with recombination occurring more frequently within than between them. That suggests the existence of a barrier to gene flow, which further maintains divergence. Genomic regions of high population differentiation harbored genes associated with possible adaptations to high/low light conditions and stress stimuli, although with a weak diversifying selection. Overall, the diversification of Laspinema species might have been affected by both genomic and ecological processes.

Zobrazit více v PubMed

Bankevich A., Nurk S., Antipov D., Gurevich A. A., Dvorkin M., Kulikov A. S., et al. . (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477. doi: 10.1089/cmb.2012.0021, PMID: PubMed DOI PMC

Barraclough T. G., Balbi K. J., Ellis R. J. (2012). Evolving concepts of bacterial species. Evol. Biol. 39, 148–157. doi: 10.1007/s11692-012-9181-8 DOI

Bobay L. M. (2020). “The prokaryotic species concept and challenges,” in The Pangenome. eds. Tettelin H., Medini D. (Cham: Springer; ), 21–49. PubMed

Bobay L. M., Ochman H. (2017). Biological species are universal across life's domains. Genome Biol. Evol. 9, 491–501. doi: 10.1093/gbe/evx026, PMID: PubMed DOI PMC

Bolger A. M., Lohse M., Usadel B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120. doi: 10.1093/bioinformatics/btu170, PMID: PubMed DOI PMC

Cadillo-Quiroz H., Didelot X., Held N. L., Herrera A., Darling A., Reno M. L., et al. . (2012). Patterns of gene flow define species of thermophilic archaea. PLoS Biol. 10:e1001265. doi: 10.1371/journal.pbio.1001265, PMID: PubMed DOI PMC

Carrolo M., Pinto F. R., Melo-Cristino J., Ramirez M. (2009). Pherotypes are driving genetic differentiation within Streptococcus pneumoniae. BMC Microbiol. 9, 1–10. doi: 10.1186/1471-2180-9-191, PMID: PubMed DOI PMC

Casamatta D. A., Vis M. L., Sheath R. G. (2003). Cryptic species in cyanobacterial systematics: a case study of Phormidium retzii (Oscillatoriales) using RAPD molecular markers and 16S rDNA sequence data. Aquat. Bot. 77, 295–309. doi: 10.1016/j.aquabot.2003.08.005 DOI

Chaguza C., Andam C. P., Harris S. R., Cornick J. E., Yang M., Bricio-Moreno L., et al. . (2016). Recombination in Streptococcus pneumoniae lineages increase with carriage duration and size of the polysaccharide capsule. MBio 7, e01053–e01016. doi: 10.1128/mBio.01053-16, PMID: PubMed DOI PMC

Chase A. B., Arevalo P., Brodie E. L., Polz M. F., Karaoz U., Martiny J. B. (2019). Maintenance of sympatric and allopatric populations in free-living terrestrial bacteria. MBio 10, e02361–e02319. doi: 10.1128/mBio.02361-19, PMID: PubMed DOI PMC

Coleman M. L., Chisholm S. W. (2010). Ecosystem-specific selection pressures revealed through comparative population genomics. Proc. Natl. Acad. Sci. U. S. A. 107, 18634–18639. doi: 10.1073/pnas.1009480107, PMID: PubMed DOI PMC

Cordero O. X., Ventouras L. A., DeLong E. F., Polz M. F. (2012). Public good dynamics drive evolution of iron acquisition strategies in natural bacterioplankton populations. Proc. Natl. Acad. Sci. U. S. A. 109, 20059–20064. doi: 10.1073/pnas.1213344109, PMID: PubMed DOI PMC

Croucher N. J., Page A. J., Connor T. R., Delaney A. J., Keane J. A., Bentley S. D., et al. . (2015). Rapid phylogenetic analysis of large samples of recombinant bacterial whole genome sequences using Gubbins. Nucleic Acids Res. 43:e15. doi: 10.1093/nar/gku1196, PMID: PubMed DOI PMC

Danecek P., Auton A., Abecasis G., Albers C. A., Banks E., DePristo M. A., et al. . (2011). The variant call format and VCFtools. Bioinformatics 27, 2156–2158. doi: 10.1093/bioinformatics/btr330, PMID: PubMed DOI PMC

Duval C., Hamlaoui S., Piquet B., Toutirais G., Yepremian C., Reinhart A., et al. . (2020). Characterization of cyanobacteria isolated from thermal muds of Balaruc-les-Bains (France) and description of a new genus and species Pseudochroococcus couteii. bioRxiv. doi: 10.1101/2020.12.12.422513 PubMed DOI PMC

Dvořák P., Casamatta D. A., Hašler P., Jahodářová E., Norwich A. R., Poulíčková A. (2017). “Diversity of the cyanobacteria,” in Modern Topics in the Phototrophic Prokaryotes. ed. Hallenbeck P. C. (Cham: Springer; ), 3–46.

Dvořák P., Casamatta D. A., Poulíčková A., Hašler P., Ondřej V., Sanges R. (2014). Synechococcus: 3 billion years of global dominance. Mol. Ecol. 23, 5538–5551. doi: 10.1111/mec.12948, PMID: PubMed DOI

Dvořák P., Poulíčková A., Hašler P., Belli M., Casamatta D. A., Papini A. (2015). Species concepts and speciation factors in cyanobacteria, with connection to the problems of diversity and classification. Biodivers. Conserv. 24, 739–757. doi: 10.1007/s10531-015-0888-6 DOI

Edgar R. C. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32, 1792–1797. doi: 10.1093/nar/gkh340, PMID: PubMed DOI PMC

Emms D. M., Kelly S. (2019). OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 20, 238–214. doi: 10.1186/s13059-019-1832-y, PMID: PubMed DOI PMC

Felsenstein J. (2005). PHYLIP: Phylogeny Inference Package, Version 3.6. Seattle, WA: University of Washington.

Fraser C., Hanage W. P., Spratt B. G. (2007). Recombination and the nature of bacterial speciation. Science 315, 476–480. doi: 10.1126/science.1127573, PMID: PubMed DOI PMC

Galtier N., Daubin V. (2008). Dealing with incongruence in phylogenomic analyses. Philos. Trans. R. Soc. B Biol. Sci. 363, 4023–4029. doi: 10.1098/rstb.2008.0144, PMID: PubMed DOI PMC

González-Torres P., Rodríguez-Mateos F., Antón J., Gabaldón T. (2019). Impact of homologous recombination on the evolution of prokaryotic core genomes. MBio 10, e02494–e02418. doi: 10.1128/mBio.02494-18, PMID: PubMed DOI PMC

Goris J., Konstantinidis K. T., Klappenbach J. A., Coenye T., Vandamme P., Tiedje J. M. (2007). DNA–DNA hybridization values and their relationship to whole-genome sequence similarities. Int. J. Syst. Evol. Microbiol. 57, 81–91. doi: 10.1099/ijs.0.64483-0, PMID: PubMed DOI

Grundmann G. L. (2004). Spatial scales of soil bacterial diversity – the size of a clone. FEMS Microbiol. Ecol. 48, 119–127. doi: 10.1016/j.femsec.2004.01.010, PMID: PubMed DOI

Hadfield J., Croucher N. J., Goater R. J., Abudahab K., Aanensen D. M., Harris S. R. (2018). Phandango: an interactive viewer for bacterial population genomics. Bioinformatics 34, 292–293. doi: 10.1093/bioinformatics/btx610, PMID: PubMed DOI PMC

Harris H. M. B., Bourin M. J. B., Claesson M. J., O'Toole P. W. (2017). Phylogenomics and comparative genomics of lactobacillus salivarius, a mammalian gut commensal. Microb. Genom. 3:e000115. doi: 10.1099/mgen.0.000115, PMID: PubMed DOI PMC

Hašler P., Dvořák P., Johansen J. R., Kitner M., Ondřej V., Poulíčková A. (2012). Morphological and molecular study of epipelic filamentous genera Phormidium, microcoleus and Geitlerinema (Oscillatoriales, Cyanophyta/cyanobacteria). Fottea 12, 341–356. doi: 10.5507/fot.2012.024 DOI

Heidari F., Hauer T., Zima J. R. H., Riahi H. (2018). New simple trichal cyanobacterial taxa isolated from radioactive thermal springs. Fottea 18, 137–149. doi: 10.5507/fot.2017.024 DOI

Held N. L., Herrera A., Cadillo-Quiroz H., Whitaker R. J. (2010). CRISPR associated diversity within a population of Sulfolobus islandicus. PLoS One 5:e12988. doi: 10.1371/journal.pone.0012988, PMID: PubMed DOI PMC

Hoang D. T., Chernomor O., Von Haeseler A., Minh B. Q., Vinh L. S. (2018). UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35, 518–522. doi: 10.1093/molbev/msx281, PMID: PubMed DOI PMC

Hunt D. E., David L. A., Gevers D., Preheim S. P., Alm E. J., Polz M. F. (2008). Resource partitioning and sympatric differentiation among closely related bacterioplankton. Science 320, 1081–1085. doi: 10.1126/science.1157890, PMID: PubMed DOI

Huson D. H., Bryant D. (2006). Application of phylogenetic networks in evolutionary studies. Mol. Biol. Evol. 23, 254–267. doi: 10.1093/molbev/msj030 PubMed DOI

Jaspers E., Overmann J. (2004). Ecological significance of microdiversity: identical 16S rRNA gene sequences can be found in bacteria with highly divergent genomes and ecophysiologies. Appl. Environ. Microbiol. 70, 4831–4839. doi: 10.1128/AEM.70.8.4831-4839.2004, PMID: PubMed DOI PMC

Jeltsch A. (2003). Maintenance of species identity and controlling speciation of bacteria: a new function for restriction/modification systems? Gene 317, 13–16. doi: 10.1016/S0378-1119(03)00652-8, PMID: PubMed DOI

Kalyaanamoorthy S., Minh B. Q., Wong T. K. F., von Haeseler A., Jermiin L. S. (2017). ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589. doi: 10.1038/nmeth.4285, PMID: PubMed DOI PMC

Kashtan N., Roggensack S. E., Rodrigue S., Thompson J. W., Biller S. J., Coe A., et al. . (2014). Single-cell genomics reveals hundreds of coexisting subpopulations in wild Prochlorococcus. Science 344, 416–420. doi: 10.1126/science.1248575, PMID: PubMed DOI

Kollár J., Poulíčková A., Dvořák P. (2022). On the relativity of species, or the probabilistic solution to the species problem. Mol. Ecol. 31, 411–418. doi: 10.1111/mec.16218, PMID: PubMed DOI

Komárek J., Anagnostidis K. (2005). “Cyanoprokaryota 2. Teil: oscillatoriales,” in Süsswasserflora von Mitteleuropa. eds. Büdel B., Gärdner G., Krienitz L., Schagerl M. (München: Elsevier; ), 759.

Koonin E. V., Makarova K. S., Wolf Y. I. (2021). Evolution of microbial genomics: conceptual shifts over a quarter century. Trends Microbiol. 29, 582–592. doi: 10.1016/j.tim.2021.01.005, PMID: PubMed DOI PMC

Korber B. (2000). “HIV signature and sequence variation analysis,” in Computational Analysis of HIV Molecular Sequences. eds. Rodrigo A. G., Learn G. H. (Dordrecht: Kluwer Academic Publishers; ), 55–72.

Larsson A. (2014). AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics 30, 3276–3278. doi: 10.1093/bioinformatics/btu531, PMID: PubMed DOI PMC

Li H., Durbin R. (2009). Fast and accurate short read alignment with burrows–wheeler transform. Bioinformatics 25, 1754–1760. doi: 10.1093/bioinformatics/btp324, PMID: PubMed DOI PMC

Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., et al. . (2009). The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079. doi: 10.1093/bioinformatics/btp352, PMID: PubMed DOI PMC

Mager D. M., Thomas A. D. (2011). Extracellular polysaccharides from cyanobacterial soil crusts: a review of their role in dryland soil processes. J. Arid Environ. 75, 91–97. doi: 10.1016/j.jaridenv.2010.10.001 DOI

Martin S. H., Dasmahapatra K. K., Nadeau N. J., Salazar C., Walters J. R., Simpson F., et al. . (2013). Genome-wide evidence for speciation with gene flow in Heliconius butterflies. Genome Res. 23, 1817–1828. doi: 10.1101/gr.159426.113, PMID: PubMed DOI PMC

Martin D. P., Lemey P., Posada D. (2011). Analysing recombination in nucleotide sequences. Mol. Ecol. Resour. 11, 943–955. doi: 10.1111/j.1755-0998.2011.03026.x PubMed DOI

Martinez-Urtaza J., Van Aerle R., Abanto M., Haendiges J., Myers R. A., Trinanes J., et al. . (2017). Genomic variation and evolution of Vibrio parahaemolyticus ST36 over the course of a transcontinental epidemic expansion. MBio 8, e01425–e01417. doi: 10.1128/mBio.01425-17, PMID: PubMed DOI PMC

Mayr E. (1942). Systematics and the Origin of Species. New York, NY: Columbia University Press.

McInerney J. O., McNally A., O'connell M. J. (2017). Why prokaryotes have pangenomes. Nat. Microbiol. 2, 1–5. doi: 10.1038/nmicrobiol.2017.40 PubMed DOI

McKenna A., Hanna M., Banks E., Sivachenko A., Cibulskis K., Kernytsky A., et al. . (2010). The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297–1303. doi: 10.1101/gr.107524.110, PMID: PubMed DOI PMC

Mirarab S., Warnow T. (2015). ASTRAL-II: coalescent-based species tree estimation with many hundreds of taxa and thousands of genes. Bioinformatics 31, i44–i52. doi: 10.1093/bioinformatics/btv234, PMID: PubMed DOI PMC

Nguyen L. T., Schmidt H. A., von Haeseler A., Minh B. Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274. doi: 10.1093/molbev/msu300, PMID: PubMed DOI PMC

Page A. J., Cummins C. A., Hunt M., Wong V. K., Reuter S., Holden M. T. G., et al. . (2015). Roary: rapid large-scale prokaryote pan genome analysis. Bioinformatics 31, 3691–3693. doi: 10.1093/bioinformatics/btv421, PMID: PubMed DOI PMC

Parks D. H., Imelfort M., Skennerton C. T., Hugenholtz P., Tyson G. W. (2015). Check M: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055. doi: 10.1101/gr.186072.114, PMID: PubMed DOI PMC

Pérez-Carrascal O. M., Terrat Y., Giani A., Fortin N., Greer C. W., Tromas N., et al. . (2019). Coherence of Microcystis species revealed through population genomics. ISME J. 13, 2887–2900. doi: 10.1038/s41396-019-0481-1, PMID: PubMed DOI PMC

Pfeifer B., Wittelsbürger U., Ramos-Onsins S. E., Lercher M. J. (2014). PopGenome: an efficient Swiss army knife for population genomic analyses in R. Mol. Biol. Evol. 31, 1929–1936. doi: 10.1093/molbev/msu136, PMID: PubMed DOI PMC

Pietrasiak N., Mühlsteinová R., Siegesmund M. A., Johansen J. R. (2014). Phylogenetic placement of Symplocastrum (Phormidiaceae, Cyanophyceae) with a new combination S. californicum and two new species: S. flechtnerae and S. torsivum. Phycologia 53, 529–541. doi: 10.2216/14-029.1 DOI

Pietrasiak N., Osorio-Santos K., Shalygin S., Martin M. P., Johansen J. R. (2019). When is a lineage a species? A case study in Myxacorys gen. Nov.(Synechococcales: cyanobacteria) with the description of two new species from the Americas. J. Phycol. 55, 976–996. doi: 10.1111/jpy.12897, PMID: PubMed DOI

Polz M. F., Alm E. J., Hanage W. P. (2013). Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends Genet. 29, 170–175. doi: 10.1016/j.tig.2012.12.006, PMID: PubMed DOI PMC

Purcell S., Neale B., Todd-Brown K., Thomas L., Ferreira M. A., Bender D., et al. . (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559–575. doi: 10.1086/519795, PMID: PubMed DOI PMC

R Core Team (2021). R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing.

Rambaut A. (2012). FigTree, version 1.4.4, pp. Computer Program Distributed by the Author. Available at: http://tree.bio.ed.ac.uk/software/figtree/ (Accessed January 10, 2022).

Raudvere U., Kolberg L., Kuzmin I., Arak T., Adler P., Peterson H., et al. . (2019). G:profiler: a web server for functional enrichment analysis and conversions of gene lists (2019 update). Nucleic Acids Res. 47, W191–W198. doi: 10.1093/nar/gkz369, PMID: PubMed DOI PMC

Reno M. L., Held N. L., Fields C. J., Burke P. V., Whitaker R. J. (2009). Biogeography of the Sulfolobus islandicus pan-genome. Proc. Natl. Acad. Sci. U. S. A. 106, 8605–8610. doi: 10.1073/pnas.0808945106, PMID: PubMed DOI PMC

Richter M., Rosselló-Móra R. (2009). Shifting the genomic gold standard for the prokaryotic species definition. Proc. Natl. Acad. Sci. U. S. A. 106, 19126–19131. doi: 10.1073/pnas.0906412106, PMID: PubMed DOI PMC

Rocap G., Larimer F. W., Lamerdin J., Malfatti S., Chain P., Ahlgren N. A., et al. . (2003). Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 424, 1042–1047. doi: 10.1038/nature01947, PMID: PubMed DOI

Rodriguez-Valera F., Martin-Cuadrado A. B., López-Pérez M. (2016). Flexible genomic islands as drivers of genome evolution. Curr. Opin. Microbiol. 31, 154–160. doi: 10.1016/j.mib.2016.03.014, PMID: PubMed DOI

Rodriguez-Valera F., Ussery D. W. (2012). Is the pan-genome also a pan-selectome? F1000Research 1:16. doi: 10.12688/f1000research.1-16.v1 PubMed DOI PMC

Roux C., Fraisse C., Romiguier J., Anciaux Y., Galtier N., Bierne N. (2016). Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biol. 14:e2000234. doi: 10.1371/journal.pbio.2000234, PMID: PubMed DOI PMC

Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J. C., Guirao-Rico S., Librado P., Ramos-Onsins S. E., et al. . (2017). DnaSP 6: DNA sequence polymorphism analysis of large datasets. Mol. Biol. Evol. 34, 3299–3302. doi: 10.1093/molbev/msx248, PMID: PubMed DOI

Seemann T. (2014). Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069. doi: 10.1093/bioinformatics/btu153, PMID: PubMed DOI

Shapiro B. J., Friedman J., Cordero O. X., Preheim S. P., Timberlake S. C., Szabó G., et al. . (2012). Population genomics of early events in the ecological differentiation of bacteria. Science 336, 48–51. doi: 10.1126/science.1218198 PubMed DOI PMC

Shapiro B. J., Polz M. F. (2014). Ordering microbial diversity into ecologically and genetically cohesive units. Trends Microbiol. 22, 235–247. doi: 10.1016/j.tim.2014.02.006, PMID: PubMed DOI PMC

Shapiro B. J., Polz M. F. (2015). Microbial speciation. Cold Spring Harb. Perspect. Biol. 7:a018143. doi: 10.1101/cshperspect.a018143, PMID: PubMed DOI PMC

Sheinman M., Arkhipova K., Arndt P. F., Dutilh B. E., Hermsen R., Massip F. (2021). Identical sequences found in distant genomes reveal frequent horizontal transfer across the bacterial domain. elife 10:e62719. doi: 10.7554/eLife.62719, PMID: PubMed DOI PMC

Simmons S. L., DiBartolo G., Denef V. J., Goltsman D. S. A., Thelen M. P., Banfield J. F. (2008). Population genomic analysis of strain variation in Leptospirillum group II bacteria involved in acid mine drainage formation. PLoS Biol. 6:e177. doi: 10.1371/journal.pbio.0060177, PMID: PubMed DOI PMC

Stanojković A., Skoupý S., Hašler P., Poulíčková A., Dvořák P. (2022). Geography and climate drive the distribution and diversification of the cosmopolitan cyanobacterium microcoleus (Oscillatoriales, cyanobacteria). Eur. J. Phycol. 1–10, 1–10. doi: 10.1080/09670262.2021.2007420 DOI

Staub R. (1961). Ernährungsphysiologisch-autökologische Untersuchungen an der planktischen Blaualge Oscillatoria rubescens DC. Schweiz. Z. Hydrol. 23, 82–198.

Stuart R. K., Brahamsha B., Busby K., Palenik B. (2013). Genomic island genes in a coastal marine Synechococcus strain confer enhanced tolerance to copper and oxidative stress. ISME J. 7, 1139–1149. doi: 10.1038/ismej.2012.175, PMID: PubMed DOI PMC

Suyama M., Torrents D., Bork P. (2006). PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 34, W609–W612. doi: 10.1093/nar/gkl315, PMID: PubMed DOI PMC

Tamura K., Stecher G., Kumar S. (2021). MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027. doi: 10.1093/molbev/msab120, PMID: PubMed DOI PMC

Törönen P., Medlar A., Holm L. (2018). PANNZER2: a rapid functional annotation web server. Nucleic Acids Res. 46, W84–W88. doi: 10.1093/nar/gky350, PMID: PubMed DOI PMC

Vos M., Didelot X. (2009). A comparison of homologous recombination rates in bacteria and archaea. ISME J. 3, 199–208. doi: 10.1038/ismej.2008.93, PMID: PubMed DOI

Vos M., Wolf A. B., Jennings S. J., Kowalchuk G. A. (2013). Micro-scale determinants of bacterial diversity in soil. FEMS Microbiol. Rev. 37, 936–954. doi: 10.1111/1574-6976.12023, PMID: PubMed DOI

Walk S. T. (2015). The “cryptic” Escherichia. EcoSal Plus 6. doi: 10.1128/ecosalplus.ESP-0002-2015 PubMed DOI PMC

Ward D. M., Cohan F. M., Bhaya D., Heidelberg J. F., Kühl M., Grossman A. (2008). Genomics, environmental genomics and the issue of microbial species. Heredity 100, 207–219. doi: 10.1038/sj.hdy.6801011 PubMed DOI

Warnes M. G. R., Bolker B., Bonebakker L., Gentleman R., Huber W. (2016). Package 'gplots'. Various R Programming Tools for Plotting data.

Wickham H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York: Springer-Verlag.

Wiedenbeck J., Cohan F. M. (2011). Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol. Rev. 35, 957–976. doi: 10.1111/j.1574-6976.2011.00292.x, PMID: PubMed DOI

Wielgoss S., Didelot X., Chaudhuri R. R., Liu X., Weedall G. D., Velicer G. J., et al. . (2016). A barrier to homologous recombination between sympatric strains of the cooperative soil bacterium Myxococcus xanthus. ISME J. 10, 2468–2477. doi: 10.1038/ismej.2016.34, PMID: PubMed DOI PMC

Wu Y. W., Simmons B. A., Singer S. W. (2016). Max bin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607. doi: 10.1093/bioinformatics/btv638, PMID: PubMed DOI

Yarza P., Yilmaz P., Pruesse E., Glöckner F. O., Ludwig W., Schleifer K. H., et al. . (2014). Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat. Rev. Microbiol. 12, 635–645. doi: 10.1038/nrmicro3330, PMID: PubMed DOI

Zamani N., Russell P., Lantz H., Hoeppner M. P., Meadows J. R., Vijay N., et al. . (2013). Unsupervised genome-wide recognition of local relationship patterns. BMC Genomics 14, 1–11. doi: 10.1186/1471-2164-14-347, PMID: PubMed DOI PMC

Zamudio R., Haigh R. D., Ralph J. D., De Ste Croix M., Tasara T., Zurfluh K., et al. . (2020). Lineage-specific evolution and gene flow in listeria monocytogenes are independent of bacteriophages. Environ. Microbiol. 22, 5058–5072. doi: 10.1111/1462-2920.15111, PMID: PubMed DOI PMC

Zhang C., Rabiee M., Sayyari E., Mirarab S. (2018). ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinform. 19, 153. doi: 10.1186/s12859-018-2129-y, PMID: PubMed DOI PMC

Zhaxybayeva O., Doolittle W. F., Papke R. T., Gogarten J. P. (2009). Intertwined evolutionary histories of marine Synechococcus and Prochlorococcus marinus. Genome Biol. Evol. 1, 325–339. doi: 10.1093/gbe/evp032, PMID: PubMed DOI PMC

Zimba P. V., Shalygin S., Huang I. S., Momčilović M., Abdulla H. (2020). A new boring toxin producer – Perforafilum tunnelli gen. & sp. nov.(Oscillatoriales, Cyanobacteria) isolated from Laguna Madre, Texas, USA. Phycologia 60, 10–24. doi: 10.1080/00318884.2020.1808389, PMID: PubMed DOI

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.20116118

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace