Niche-directed evolution modulates genome architecture in freshwater Planctomycetes

. 2019 Apr ; 13 (4) : 1056-1071. [epub] 20190104

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid30610231
Odkazy

PubMed 30610231
PubMed Central PMC6461901
DOI 10.1038/s41396-018-0332-5
PII: 10.1038/s41396-018-0332-5
Knihovny.cz E-zdroje

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).

Zobrazit více v PubMed

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

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Integrating depth-dependent protist dynamics and microbial interactions in spring succession of a freshwater reservoir

. 2024 May 08 ; 19 (1) : 31. [epub] 20240508

Freshwater genome-reduced bacteria exhibit pervasive episodes of adaptive stasis

. 2024 Apr 23 ; 15 (1) : 3421. [epub] 20240423

Global freshwater distribution of Telonemia protists

. 2024 Jan 08 ; 18 (1) : .

In the right place, at the right time: the integration of bacteria into the Plankton Ecology Group model

. 2023 May 20 ; 11 (1) : 112. [epub] 20230520

Postglacial adaptations enabled colonization and quasi-clonal dispersal of ammonia-oxidizing archaea in modern European large lakes

. 2023 Feb 03 ; 9 (5) : eadc9392. [epub] 20230201

Diversity dynamics of aerobic anoxygenic phototrophic bacteria in a freshwater lake

. 2023 Feb ; 15 (1) : 60-71. [epub] 20221212

High-resolution metagenomic reconstruction of the freshwater spring bloom

. 2023 Jan 26 ; 11 (1) : 15. [epub] 20230126

The Evolutionary Kaleidoscope of Rhodopsins

. 2022 Oct 26 ; 7 (5) : e0040522. [epub] 20220919

Photoheterotrophy by aerobic anoxygenic bacteria modulates carbon fluxes in a freshwater lake

. 2022 Apr ; 16 (4) : 1046-1054. [epub] 20211120

Heliorhodopsin Evolution Is Driven by Photosensory Promiscuity in Monoderms

. 2021 Dec 22 ; 6 (6) : e0066121. [epub] 20211124

Expanded Diversity and Metabolic Versatility of Marine Nitrite-Oxidizing Bacteria Revealed by Cultivation- and Genomics-Based Approaches

. 2020 Oct 28 ; 86 (22) : . [epub] 20201028

Visualization of Lokiarchaeia and Heimdallarchaeia (Asgardarchaeota) by Fluorescence In Situ Hybridization and Catalyzed Reporter Deposition (CARD-FISH)

. 2020 Jul 29 ; 5 (4) : . [epub] 20200729

Light and Primary Production Shape Bacterial Activity and Community Composition of Aerobic Anoxygenic Phototrophic Bacteria in a Microcosm Experiment

. 2020 Jul 01 ; 5 (4) : . [epub] 20200701

Phage-centric ecological interactions in aquatic ecosystems revealed through ultra-deep metagenomics

. 2019 Oct 20 ; 7 (1) : 135. [epub] 20191020

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...