Niche-directed evolution modulates genome architecture in freshwater Planctomycetes
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
30610231
PubMed Central
PMC6461901
DOI
10.1038/s41396-018-0332-5
PII: 10.1038/s41396-018-0332-5
Knihovny.cz E-zdroje
- MeSH
- Bacteria klasifikace genetika MeSH
- ekosystém MeSH
- fylogeneze MeSH
- genom bakteriální * MeSH
- genomika MeSH
- molekulární evoluce * MeSH
- sladká voda mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Freshwater environments teem with microbes that do not have counterparts in culture collections or genetic data available in genomic repositories. Currently, our apprehension of evolutionary ecology of freshwater bacteria is hampered by the difficulty to establish organism models for the most representative clades. To circumvent the bottlenecks inherent to the cultivation-based techniques, we applied ecogenomics approaches in order to unravel the evolutionary history and the processes that drive genome architecture in hallmark freshwater lineages from the phylum Planctomycetes. The evolutionary history inferences showed that sediment/soil Planctomycetes transitioned to aquatic environments, where they gave rise to new freshwater-specific clades. The most abundant lineage was found to have the most specialised lifestyle (increased regulatory genetic circuits, metabolism tuned for mineralization of proteinaceous sinking aggregates, psychrotrophic behaviour) within the analysed clades and to harbour the smallest freshwater Planctomycetes genomes, highlighting a genomic architecture shaped by niche-directed evolution (through loss of functions and pathways not needed in the newly acquired freshwater niche).
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Woese CR, Stackebrandt E, Macke TJ, Fox GE. A phylogenetic definition of the major eubacterial taxa. Syst Appl Microbiol. 1985;6:143–51. PubMed
Staley JT. Budding bacteria of the Pasteuria–Blastobacter group. Can J Microbiol. 1973;19:609–14. PubMed
Garrity George M., Holt John G. Bergey’s Manual® of Systematic Bacteriology. New York, NY: Springer New York; 2001. The Road Map to the Manual; pp. 119–166.
Erko S, Ludvig W, Schubert W, Klink F, Schlesner H, et al. Molecular genetic evidence for early evolutionary origin of budding peptidoglycan-less Eubacteria. Nature. 1984;307:735–7357. PubMed
Devos DP, Reynaud EG. Intermediate steps. Science (80-) 2010;330:1187–8. PubMed
Fuerst JA, Sagulenko E. Beyond the bacterium: Planctomycetes challenge our concepts of microbial structure and function. Nat Rev Microbiol. 2011;9:403–13. PubMed
Gimesi. I Planctomyces Bekefii Gim. nov. gen. et sp. (Ein neues Glied des Phytoplanktons.). Hydrobiologiai Tanulmiinyok (Hydrobiologische Studien). Budapest: Kiadja a Magyar Ciszterci Rend; 1924.
Hirsch P. Two identical genera of budding and stalked bacteria: Planctomyces Gimesi 1924 and Blastocaulis Henrici and Johnson 1935. Int J Syst Bacteriol. 1972;22:107–11.
Bauld J, Staley TJ. Planctomyces maris sp. nov.: a marine isolate of the planctomyces-blastocaulis group of budding bacteria. Microbiology. 1976;97:45–55.
Schmidt JM, Starr MP. Morphological diversity of freshwater bacteria belonging to the Blastocaulis-planctomyces group as observed in natural populations and enrichments. Curr Microbiol. 1978;1:325–30.
Schlesner H, Rensmann C, Tindall BJ, Gade D, Rabus R, Pfeiffer S, et al. Taxonomic heterogeneity within the Planctomycetales as derived by DNA-DNA hybridization, description of Rhodopirellula baltica gen. nov., sp. nov., transfer of Perillula marina to the genus Blastopirellula gen. nov. as Blastopirellula marina comb. nov. an. Int J Syst Evol Microbiol. 2004;54:1567–80. PubMed
Fukunaga Y, Kurahashi M, Sakiyama Y, Ohuchi M, Yokota A, Harayama S. Phycisphaera mikurensis gen. nov., sp. nov., isolated from a marine alga, and proposal of Phycisphaeraceae fam. nov., Phycisphaerales ord. nov. and Phycisphaerae classis nov. in the phylum Planctomycetes. J Gen Appl Microbiol. 2009;55:267–75. PubMed
Lindsay MR, Webb RI, Fuerst JA. Pirellulosomes: a new type of membrane-bounded cell compartment in planctomycete bacteria of the genus pirellula. Microbiology. 1997;143:739–48. PubMed
König E, Schlesner H, Hirsch P. Cell wall studies on budding bacteria of the Planctomyces/Pasteuria group and on a Prosthecomicrobium sp. Arch Microbiol. 1984;138:200–5.
Lonhienne TGA, Sagulenko E, Webb RI, Lee KC, Franke J, Devos DP, et al. Endocytosis-like protein uptake in the bacterium Gemmata obscuriglobus. Proc Natl Acad Sci. 2010;107:12883–8. PubMed PMC
Glockner FO, Kube M, Bauer M, Teeling H, Lombardot T, Ludwig W, et al. Complete genome sequence of the marine planctomycete Pirellula sp. strain 1. Proc Natl Acad Sci. 2003;100:8298–303. PubMed PMC
Guo M, Zhou Q, Zhou Y, Yang L, Liu T, Yang J, et al. Genomic evolution of 11 type strains within family Planctomycetaceae. PLoS ONE. 2014;9:e86752. PubMed PMC
Delmont TO, Quince C, Shaiber A, Esen OC, Lee STM, Lucker S, et al. Nitrogen-fixing populations of planctomycetes and Proteobacteria are abundant in the surface ocean. bioRxiv. 2017;3:129791. PubMed
Reva O, Tümmler B. Think big - Giant genes in bacteria. Environ Microbiol. 2008;10:768–77. PubMed
Mcinerney JO, Martin WF, Koonin EV, Allen JF, Galperin MY, Lane N, et al. Planctomycetes and eukaryotes: a case of analogy not homology. Bioessays. 2011;33:810–7. PubMed PMC
Boedeker C, Schüler M, Reintjes G, Jeske O, Van Teeseling MCF, Jogler M, et al. Determining the bacterial cell biology of Planctomycetes. Nat Commun. 2017;8:14853. PubMed PMC
Jeske O, Schüler M, Schumann P, Schneider A, Boedeker C, Jogler M, et al. Planctomycetes do possess a peptidoglycan cell wall. Nat Commun. 2015;6:7116. PubMed PMC
Neef A, Amann R, Schlesner H, Schleifer KH. Monitoring a widespread bacterial group: in situ detection of planctomycetes with 16S rRNA-targeted probes. Microbiology. 1998;144:3257–66. PubMed
Gade D, Schlesner H, Glockner FO, Amann R, Pfeiffer S, Thomm M. Identification of Planctomycetes with order-, genus-, and strain-specific 16S rRNA-targeted probes. Microb Ecol. 2004;47:243–51. PubMed
Buckley DH, Huangyutitham V, Nelson TA, Rumberger A, Thies JE. Diversity of Planctomycetes in soil in relation to soil history and environmental heterogeneity. Appl Environ Microbiol. 2006;72:4522–31. PubMed PMC
Ivanova AA, Kulichevskaya IS, Merkel AY, Toshchakov SV, Dedysh SN. High diversity of planctomycetes in soils of two lichen-dominated sub-arctic ecosystems of Northwestern Siberia. Front Microbiol. 2016;7:1–13. PubMed PMC
Okazaki Y, Fujinaga S, Tanaka A, Kohzu A, Oyagi H, Nakano SI. Ubiquity and quantitative significance of bacterioplankton lineages inhabiting the oxygenated hypolimnion of deep freshwater lakes. ISME J. 2017;11:2279–93. PubMed PMC
Lage OM, Bondoso J. Bringing Planctomycetes into pure culture. Front Microbiol. 2012;3:1–6. PubMed PMC
Reintjes G, Arnosti C, Fuchs BM, Amann R. An alternative polysaccharide uptake mechanism of marine bacteria. ISME J. 2017;11:1640–50. PubMed PMC
Ntougias S, Polkowska Ż, Nikolaki S, Dionyssopoulou E, Stathopoulou P, Doudoumis V, et al. Bacterial community structures in freshwater polar environments of Svalbard. Microbes Environ. 2016;31:401–9. PubMed PMC
Okazaki Y, Nakano SI. Vertical partitioning of freshwater bacterioplankton community in a deep mesotrophic lake with a fully oxygenated hypolimnion (Lake Biwa, Japan) Environ Microbiol Rep. 2016;8:780–8. PubMed
Karlov DS, Marie D, Sumbatyan DA, Chuvochina MS, Kulichevskaya IS, Alekhina IA, et al. Microbial communities within the water column of freshwater Lake Radok, East Antarctica: predominant 16S rDNA phylotypes and bacterial cultures. Polar Biol. 2017;40:823–36.
Tadonléké RD. Strong coupling between natural Planctomycetes and changes in the quality of dissolved organic matter in freshwater samples. FEMS Microbiol Ecol. 2007;59:543–55. PubMed
Hirsch P, Müller M. Planctomyces limnophilus sp. nov., a stalked and budding bacterium from freshwater. Syst Appl Microbiol. 1985;6:276–80.
Labutti K, Sikorski J, Schneider S, Nolan M, Lucas S, del Rio TG, et al. Complete genome sequence of planctomyces limnophilus type strain (mü 290 T) Stand Genom Sci. 2010;3:47–56. PubMed PMC
Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK. Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquat Microb Ecol. 2002;28:141–55.
Mao DP, Zhou Q, Chen CY, Quan ZX. Coverage evaluation of universal bacterial primers using the metagenomic datasets. BMC Microbiol. 2012;12:66. PubMed PMC
Urbach E, Vergin KL, Young L, Morse A, Larson GL, Giovannoni SJ. Unusual bacterioplankton community structure in ultra-oligotrophic Crater Lake. Limnol Oceanogr. 2001;46:557–72.
Parks DH, Rinke C, Chuvochina M, Chaumeil PA, Woodcroft BJ, Evans PN, et al. Author Correction: Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat Microbiol. 2017;2:1. PubMed
Konstantinidis KT, Rosselló-Móra R, Amann R. Uncultivated microbes in need of their own taxonomy. ISME J. 2017;11:2399–406. PubMed PMC
Bowers RM, Kyrpides NC, Stepanauskas R, Harmon-Smith M, Doud D, Reddy TBK, et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat Biotechnol. 2017;35:725–31. PubMed PMC
Kuenen JG. Anammox bacteria: from discovery to application. Nat Rev Microbiol. 2008;6:320–6. PubMed
Galperin MY. A census of membrane-bound and intracellular signal transduction proteins in bacteria: Bacterial IQ, extroverts and introverts. BMC Microbiol. 2005;5:1–19. PubMed PMC
Ulrich LE, Koonin EV, Zhulin IB. One-component systems dominate signal transduction in prokaryotes. Trends Microbiol. 2005;13:52–56. PubMed PMC
Vigil-Stenman T, Ininbergs K, Bergman B, Ekman M. High abundance and expression of transposases in bacteria from the Baltic Sea. ISME J. 2017;11:2611–23. PubMed PMC
Brown CT, Olm MR, Thomas BC, Banfield JF. Measurement of bacterial replication rates in microbial communities. Nat Biotechnol. 2016;35:725–31. PubMed PMC
Gounot AM. Psychrophilic and psychrotrophie microorganisms. Experientia. 1986;42:1192–7. PubMed
Hickman JW, Tifrea DF, Harwood CS. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci. 2005;102:14422–7. PubMed PMC
Luo G, Huang L, Su Y, Qin Y, Xu X, Zhao L, et al. FlrA, flrB and flrC regulate adhesion by controlling the expression of critical virulence genes in Vibrio alginolyticus. Emerg Microbes Infect. 2016;5:e85–11. PubMed PMC
Bayer EA, Shimon LJW, Shoham Y, Lamed R. Cellulosomes - Structure and ultrastructure. J Struct Biol. 1998;124:221–34. PubMed
Artzi L, Bayer EA, Moraïs S. Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides. Nat Rev Microbiol. 2017;15:83–95. PubMed
Peer A, Smith SP, Bayer EA, Lamed R, Borovok I. Noncellulosomal cohesin- and dockin-like modules in the three domains of life. Mol Microbiol. 2011;291:1–16. PubMed PMC
Moran NA. Microbial minimalism: genome reduction in bacterial pathogens. Cell. 2002;108:583–6. PubMed
Sorensen Jackson W., Dunivin Taylor K., Tobin Tammy C., Shade Ashley. Ecological selection for small microbial genomes along a temperate-to-thermal soil gradient. Nature Microbiology. 2018;4(1):55–61. PubMed
Dufresne A, Garczarek L, Partensky F. Accelerated evolution associated with genome reduction in a free-living prokaryote. Genome Biol. 2005;6:R14. PubMed PMC
Luo H, Huang Y, Stepanauskas R, Tang J. Excess of non-conservative amino acid changes in marine bacterioplankton lineages with reduced genomes. Nat Microbiol. 2017;2:17091. PubMed
Biller SJ, Berube PM, Lindell D, Chisholm SW. Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol. 2014;13:13. PubMed
Luo H, Moran MA. How do divergent ecological strategies emerge among marine bacterioplankton lineages? Trends Microbiol. 2015;23:577–84. PubMed
Giovannoni SJ, Cameron Thrash J, Temperton B. Implications of streamlining theory for microbial ecology. ISME J. 2014;8:1553. PubMed PMC
Getz EW, Tithi SS, Zhang L, Aylward FO. Parallel evolution of genome streamlining and cellular bioenergetics across the marine radiation of a bacterial phylum. mBio. 2018;9:e01089-18. PubMed PMC
Salcher MM, Neuenschwander SM, Posch T, Pernthaler J. The ecology of pelagic freshwater methylotrophs assessed by a high-resolution monitoring and isolation campaign. ISME J. 2015;9:2442–53. PubMed PMC
Cabello-Yeves PJ, Ghai R, Mehrshad M, Picazo A, Camacho A, Rodriguez-Valera F. Reconstruction of diverse verrucomicrobial genomes from metagenome datasets of freshwater reservoirs. Front Microbiol. 2017; 8:2131. PubMed PMC
Znachor P, Nedoma J, Hejzlar J, Seďa J, Kopáček J, Boukal D, et al. Multiple long-term trends and trend reversals dominate environmental conditions in a man-made freshwater reservoir. Sci Total Environ. 2018;624:24–33. PubMed
Martín-Cuadrado AB, López-García P, Alba JC, Moreira D, Monticelli L, Strittmatter A, et al. Metagenomics of the Deep Mediterranean, a Warm Bathypelagic Habitat. PLoS ONE. 2007;2:e914. PubMed PMC
Salcher MM, Pernthaler J, Posch T. Seasonal bloom dynamics and ecophysiology of the freshwater sister clade of SAR11 bacteria that rule the waves (LD12) ISME J. 2011;5:1242–52. PubMed PMC
Bushnell B. BBDuk. 2016. https://github.com/BioInfoTools/BBMap/blob/master/sh/bbduk.sh.
Bushnell B, Rood J, Singer E. BBMerge – accurate paired shotgun read merging via overlap. PLoS ONE. 2017;12:1–15. PubMed PMC
Joshi NA, Fass J. Sickle: a sliding-window, adaptive, quality-based trimming tool for FastQ files. 2011. https://github.com/najoshi/sickle.
Bushnell B. Reformat. 2016. https://github.com/BioInfoTools/BBMap/blob/master/sh/reformat.sh.
Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26:2460–1. PubMed
Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ, et al. The ribosomal database project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 2009;37:141–5. PubMed PMC
Nawrocki E. Structural RNA homology search and alignment using covariance models. Washington: Washington University in Saint Louis, School of Medicine; 2009.
Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST:a new generation of protein database search programs. Nucleic Acids Res. 1997;25:3389–402. PubMed PMC
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Res. 2013;41:590–6. PubMed PMC
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. PubMed PMC
Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, et al. MEGAHITv1.0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11. PubMed
Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. MetaSPAdes: a new versatile metagenomic assembler. Genome Res. 2017;27:824–34. PubMed PMC
Ondov BD, Treangen TJ, Melsted P, Mallonee AB, Bergman NH, Koren S, et al. Mash: Fast genome and metagenome distance estimation using MinHash. Genome Biol. 2016;17:1–14. PubMed PMC
Bushnell B. BBMap. 2015.
Segata N, Börnigen D, Morgan XC, Huttenhower C. PhyloPhlAn is a new method for improved phylogenetic and taxonomic placement of microbes. Nat Commun. 2013;4:2304. PubMed PMC
Hyatt D, Chen GL, LoCascio PF, Land ML, Larimer FW, Hauser LJ. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics. 2010;11:119. PubMed PMC
Edgar RC. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7. PubMed PMC
Price Morgan N., Dehal Paramvir S., Arkin Adam P. FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments. PLoS ONE. 2010;5(3):e9490. PubMed PMC
Mehrshad M, Rodriguez-Valera F, Amoozegar MA, López-García P, Ghai R. The enigmatic SAR202 cluster up close: Shedding light on a globally distributed dark ocean lineage involved in sulfur cycling. ISME J. 2018;12:655–68. PubMed PMC
Konstantinidis KT, Tiedje JM. Towards a genome-based taxonomy for prokaryotes. J Bacteriol. 2005;187:6258–64. PubMed PMC
Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–9. PubMed PMC
Seemann T. Prokka: Rapid prokaryotic genome annotation. Bioinformatics. 2014;30:2068–9. PubMed
Kanehisa M, Sato Y, Morishima K. BlastKOALA and GhostKOALA: KEGG tools for functional characterization of genome and metagenome sequences. J Mol Biol. 2016;428:726–31. PubMed
Aziz RK, Bartels D, Best A, DeJongh M, Disz T, Edwards RA, et al. The RAST Server: rapid annotations using subsystems technology. BMC Genom. 2008;9:1–15. PubMed PMC
Johnson LS, Eddy SR, Portugaly E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics. 2010;11:431. PubMed PMC
Tatusov RL. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000;28:33–36. PubMed PMC
Haft DH, Selengut JD, White O. The TIGRFAMs database of protein families. Nucleic Acids Res. 2003;31:371–3. PubMed PMC
Huang L, Zhang H, Wu P, Entwistle S, Li X, Yohe T, et al. DbCAN-seq: a database of carbohydrate-active enzyme (CAZyme) sequence and annotation. Nucleic Acids Res. 2018;46:D516–D521. PubMed PMC
Finn RD, Clements J, Arndt W, Miller BL, Wheeler TJ, Schreiber F, et al. HMMER web server: 2015 Update. Nucleic Acids Res. 2015;43:W30–8. PubMed PMC
Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE. The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc. 2015;10:845. PubMed PMC
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar A, et al. ARB: A software environment for sequence data. Nucleic Acids Res. 2004;32:1363–71. PubMed PMC
Stamatakis A, Ludwig T, Meier H. RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics. 2005;21:456–63. PubMed
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30:772–80. PubMed PMC
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