Speciation Features of Ferdinandcohnia quinoae sp. nov to Adapt to the Plant Host
Jazyk angličtina Země Německo Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
SA293P18
Junta de Castilla y León
PubMed
38502221
PubMed Central
PMC10978704
DOI
10.1007/s00239-024-10164-1
PII: 10.1007/s00239-024-10164-1
Knihovny.cz E-zdroje
- Klíčová slova
- Ferdinandcohnia quinoae, Adaptation, Comparative genomics, Microbial ecology, Quinoa, Speciation,
- MeSH
- DNA bakterií genetika MeSH
- fylogeneze MeSH
- mastné kyseliny * MeSH
- RNA ribozomální 16S genetika MeSH
- rostliny * genetika MeSH
- sekvenční analýza DNA MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- DNA bakterií MeSH
- mastné kyseliny * MeSH
- RNA ribozomální 16S MeSH
The bacterial strain SECRCQ15T was isolated from seeds of Chenopodium quinoa in Spain. Phylogenetic, chemotaxonomic, and phenotypic analyses, as well as genome similarity indices, support the classification of the strain into a novel species of the genus Ferdinandcohnia, for which we propose the name Ferdinandcohnia quinoae sp. nov. To dig deep into the speciation features of the strain SECRCQ15T, we performed a comparative genomic analysis of the genome of this strain and those of the type strains of species from the genus Ferdinandcohnia. We found several genes related with plant growth-promoting mechanisms within the SECRCQ15T genome. We also found that singletons of F. quinoae SECRCQ15T are mainly related to the use of carbohydrates, which is a common trait of plant-associated bacteria. To further reveal speciation events in this strain, we revealed genes undergoing diversifying selection (e.g., genes encoding ribosomal proteins) and functions likely lost due to pseudogenization. Also, we found that this novel species contains 138 plant-associated gene-cluster functions that are unique within the genus Ferdinandcohnia. These features may explain both the ecological and taxonomical differentiation of this new taxon.
Departamento de Microbiología y Genética Universidad de Salamanca Salamanca Spain
Institute of Microbiology of the Czech Academy of Sciences Vídeňská Prague Czech Republic
Instituto de Investigación en Agrobiotecnología Universidad de Salamanca Salamanca Spain
Instituto de Recursos Naturales y Agrobiología IRNASA CSIC Salamanca Spain
Zobrazit více v PubMed
Abdelfattah A, Tack AJ, Lobato C, Wassermann B, Berg G. From seed to seed: the role of microbial inheritance in the assembly of the plant microbiome. Trends Microbiol. 2022;31(4):346–355. doi: 10.1016/j.tim.2022.10.009. PubMed DOI
Ali S, Tyagi A, Park S, Mir RA, Mushtaq M, Bhat B, et al. Deciphering the plant microbiome to improve drought tolerance: mechanisms and perspectives. Environ Exp Bot. 2022;201:104933. doi: 10.1016/j.envexpbot.2022.104933. DOI
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–410. doi: 10.1016/S0022-2836(05)80360-2. PubMed DOI
Aramaki T, Blanc-Mathieu R, Endo H, Ohkubo K, Kanehisa M, Goto S, Ogata H. KofamKOALA: KEGG Ortholog assignment based on profile HMM and adaptive score threshold. Bioinformatics. 2020;36(7):2251–2252. doi: 10.1093/bioinformatics/btz859. PubMed DOI PMC
Auch AF, von Jan M, Klenk HP, Göker M. Digital DNA-DNA hybridization for microbial species delineation by means of genome-to-genome sequence comparison. Stand Genomic Sci. 2010;2:117–134. doi: 10.4056/sigs.531120. PubMed DOI PMC
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, et al. The RAST server: rapid annotations using subsystems technology. BMC Genom. 2008;9:75. doi: 10.1186/1471-2164-9-75. PubMed DOI PMC
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol. 2012;19:455–477. doi: 10.1089/cmb.2012.0021. PubMed DOI PMC
Baquero F, Coque TM, Galán JC, Martinez JL. The origin of niches and species in the bacterial world. Front Microbiol. 2021;12:657986. doi: 10.3389/fmicb.2021.657986. PubMed DOI PMC
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, Van Wezel GP, Medema MH, Weber T. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res. 2021;49(W1):W29–W35. doi: 10.1093/nar/gkab335. PubMed DOI PMC
Carro L, Spröer C, Alonso P, Trujillo ME. Diversity of Micromonospora strains isolated from nitrogen fixing nodules and rhizosphere of Pisum sativum analyzed by multilocus sequence analysis. Syst Appl Microbiol. 2012;35:73–80. doi: 10.1016/j.syapm.2011.11.003. PubMed DOI
Cavalca L, Zanchi R, Corsini A, Colombo M, Romagnoli C, Canzi E, Andreoni V. Arsenic-resistant bacteria associated with roots of the wild Cirsium arvense (L.) plant from an arsenic polluted soil, and screening of potential plant growth-promoting characteristics. Syst Appl Microbiol. 2010;33(3):154–164. doi: 10.1016/j.syapm.2010.02.004. PubMed DOI
Chialva M, Lanfranco L, Bonfante P. The plant microbiota: composition, functions, and engineering. Curr Opin Biotechnol. 2022;73:135–142. doi: 10.1016/j.copbio.2021.07.003. PubMed DOI
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, et al. Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol. 2018;68(1):461–466. doi: 10.1099/ijsem.0.002516. PubMed DOI
Claus D, Berkeley RCW. Genus Bacillus Cohn 1872, 174AL. In: Sneath PHA, Mair NS, Sharpe ME, Holt JG, editors. Bergey’s manual of systematic bacteriology. Baltimore: Williams Wilkins; 1986. pp. 1105–1139.
Debray R, Herbert RA, Jaffe AL, Crits-Christoph A, Power ME, Koskella B. Priority effects in microbiome assembly. Nat Rev Microbiol. 2022;20(2):109–121. doi: 10.1038/s41579-021-00604-w. PubMed DOI
Ding MJ, Shang NJ, Xiao ZX, Shao F, Liu L, et al. Bacillus aciditolerans sp. nov, isolated from paddy soil. Int J Syst Evol Microbiol. 2019;69:1155–1161. doi: 10.1099/ijsem.0.003285. PubMed DOI
Doetsch RN. Determinative methods of light microscopy. In: Gerdhardt P, Murray RGE, Costilow RN, Nester EW, Wood WA, Krieg NR, Phillips GB, editors. Manual of methods for general bacteriology. Washington: American Society for Microbiology; 1981. pp. 21–33.
Dominguez-Moñino I, Jurado V, Gonzalez-Pimentel JL, Miller AZ, Hermosin B, et al. Bacillus onubensis sp. nov, isolated from the air of two Andalusian caves. Syst Appl Microbiol. 2018;41:167–172. doi: 10.1016/j.syapm.2018.01.001. PubMed DOI
Dubey A, Kumar A, Malla MA, Chowdhary K, Singh G, Gudasalamani-Ravikanth H, et al. Approaches for the amelioration of adverse effects of drought stress on crop plants. Front Biosci (landmark Ed) 2021;26(10):928–947. doi: 10.52586/4998. PubMed DOI
Eren AM, Esen ÖC, Quince C, Vineis JH, Morrison HG, Sogin ML, Delmont TO. Anvi’o: an advanced analysis and visualization platform for ‘omics data. PeerJ. 2015;3:e1319. doi: 10.7717/peerj.1319. PubMed DOI PMC
Flores-Félix JD, Silva LR, Rivera LP, Marcos-García M, García-Fraile P, et al. Plants probiotics as a tool to produce highly functional fruits: the case of Phyllobacterium and vitamin C in strawberries. PLoS ONE. 2015;10(4):e0122281. doi: 10.1371/journal.pone.0122281. PubMed DOI PMC
García-Fraile P, Menéndez E, Rivas R. Role of bacterial biofertilizers in agriculture and forestry. AIMS Bioeng. 2015;2(3):183–205. doi: 10.3934/bioeng.2015.3.183. DOI
Gomez JE, Kaufmann-Malaga BB, Wivagg CN, Kim PB, Silvis MR, et al. Ribosomal mutations promote the evolution of antibiotic resistance in a multidrug environment. Elife. 2017;6:e20420. doi: 10.7554/eLife.20420. PubMed DOI PMC
González-Dominici LI, Saati-Santamaría Z, García-Fraile P. Genome analysis and genomic comparison of the novel species Arthrobacter ipsi reveal its potential protective role in its bark beetle host. Microb Ecol. 2021;81(2):471–482. doi: 10.1007/s00248-020-01593-8. PubMed DOI
Guo J, Wang YQ, Yang G, Chen Y, Zhou S, Zhao Y, Zhuang L. Bacillus nitroreducens sp. nov, a humus-reducing bacterium isolated from a compost. Arch Microbiol. 2016;198:347–352. doi: 10.1007/s00203-016-1193-9. PubMed DOI
Gupta RS, Patel S, Saini N, Chen S. Robust demarcation of 17 distinct Bacillus species clades, proposed as novel Bacillaceae genera, by phylogenomics and comparative genomic analyses: description of Robertmurraya kyonggiensis sp. nov. and proposal for an emended genus Bacillus limiting it only to the members of the Subtilis and Cereus clades of species. Int J Syst Evol Microbiol. 2020;70:5753–5798. doi: 10.1099/ijsem.0.004475. PubMed DOI
Hartmann M, Six J. Soil structure and microbiome functions in agroecosystems. Nat Rev Earth Environ. 2023;4(1):4–18. doi: 10.1038/s43017-022-00366-w. DOI
Hemmerling F, Piel J. Strategies to access biosynthetic novelty in bacterial genomes for drug discovery. Nat Rev Drug Discov. 2022;21(5):359–378. doi: 10.1038/s41573-022-00414-6. PubMed DOI
Heyrman J, Rodriguez-Diaz M, Devos J, Felske A, Logan NA, et al. Bacillus arenosi sp. nov, Bacillus arvi sp. nov. and Bacillus humi sp. nov, isolated from soil. Int J Syst Evol Microbiol. 2005;55:111–117. doi: 10.1099/ijs.0.63240-0. PubMed DOI
Jain C, Rodriguez-R LM, Phillippy AM, Konstantinidis KT, Aluru S. High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries. Nat Commun. 2018;9(1):1–8. doi: 10.1038/s41467-018-07641-9. PubMed DOI PMC
Kalkreuter E, Pan G, Cepeda AJ, Shen B. Targeting bacterial genomes for natural product discovery. Trends Pharmacol Sci. 2020;41(1):13–26. doi: 10.1016/j.tips.2019.11.002. PubMed DOI PMC
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, et al. Introducing EzTaxon-e: a prokaryotic 16S rRNA Gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol. 2012;62:716–721. doi: 10.1099/ijs.0.038075-0. PubMed DOI
Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111–120. doi: 10.1007/BF01731581. PubMed DOI
Kokcha S, Mishra AK, Lagie JC, Million M, Leroy Q, Raoult D, Fournier PE. Non contiguous-finished genome sequence and description of Bacillus timonensis sp. nov. Stand in Genomic Sci. 2012;6:346–355. doi: 10.4056/sigs.2776064. PubMed DOI PMC
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;3:1870–1874. doi: 10.1093/molbev/msw054. PubMed DOI PMC
Laranjeira SS, Alves IG, Marques G. Chickpea (Cicer arietinum L.) seeds as a reservoir of endophytic plant growth-promoting bacteria. Curr Microbiol. 2022;79(9):277. doi: 10.1007/s00284-022-02942-1. PubMed DOI
Letunic I, Bork P. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021;49(W1):W293–W296. doi: 10.1093/nar/gkab301. PubMed DOI PMC
Levy A, Conway JM, Dangl JL, Woyke T. Elucidating bacterial gene functions in the plant microbiome. Cell Host Microbe. 2018;24(4):475–485. doi: 10.1016/j.chom.2018.09.005. PubMed DOI
Levy A, Salas Gonzalez I, Mittelviefhaus M, Clingenpeel S, Herrera Paredes S, Miao J, et al. Genomic features of bacterial adaptation to plants. Nat Genet. 2018;50(1):138–150. doi: 10.1038/s41588-017-0012-9. PubMed DOI PMC
Li E, de Jonge R, Liu C, Jiang H, Friman VP, Pieterse CM, et al. Rapid evolution of bacterial mutualism in the plant rhizosphere. Nat Commun. 2021;12(1):3829. doi: 10.1038/s41467-021-24005-y. PubMed DOI PMC
Li E, Zhang H, Jiang H, Pieterse CM, Jousset A, Bakker PA, de Jonge R. Experimental-evolution-driven identification of Arabidopsis rhizosphere competence genes in Pseudomonas protegens. Mbio. 2021;12(3):e00927–e1021. doi: 10.1128/mBio.00927-21. PubMed DOI PMC
Logan NA, Berge O, Bishop AH, Busse HJ, De Vos P, et al. Proposed minimal standards for describing new taxa of aerobic, endospore-forming bacteria. Int J Syst Evol Microbiol. 2009;59:2114–2121. doi: 10.1099/ijs.0.013649-0. PubMed DOI
McLaughlin S, Zhalnina K, Kosina S, Northen TR, Sasse J. The core metabolome and root exudation dynamics of three phylogenetically distinct plant species. Nat Commun. 2023;14(1):1649. doi: 10.1038/s41467-023-37164-x. PubMed DOI PMC
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinf. 2013;14:60. doi: 10.1186/1471-2105-14-60. PubMed DOI PMC
Na SI, Kim YO, Yoon SH, Ha SM, Baek I, Chun J. UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol. 2018;56:280–285. doi: 10.1007/s12275-018-8014-6. PubMed DOI
Nakajima T, Kawano Y, Ohtsu I, Maruyuama-Nakashita A, Allahham A, et al. Effects of thiosulfate as a sulfur source on plant growth, metabolites accumulation and gene expression in Arabidopsis and rice. Plant Cell Physiol. 2019;60(8):1683–1701. doi: 10.1093/pcp/pcz082. PubMed DOI
Nayfach S, Roux S, Seshadri R, Udwary D, Varghese N, Schulz F, et al. A genomic catalog of Earth’s microbiomes. Nat Biotechnol. 2021;39(4):499–509. doi: 10.1038/s41587-020-0718-6. PubMed DOI PMC
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 2015;25(7):1043–1055. doi: 10.1101/gr.186072.114. PubMed DOI PMC
Patz S, Gautam A, Becker M, Ruppel S, Rodríguez-Palenzuela P, Huson DH. PLaBAse: a comprehensive web resource for analyzing the plant growth-promoting potential of plant-associated bacteria. BioRxiv. 2021 doi: 10.1101/2021.12.13.472471. DOI
Peral-Aranega E, Saati-Santamaría Z, Kolařik M, Rivas R, García-Fraile P. Bacteria belonging to Pseudomonas typographi sp. nov. from the bark beetle Ips typographus have genomic potential to aid in the host ecology. InSects. 2020;11(9):593. doi: 10.3390/insects11090593. PubMed DOI PMC
Poveda J, Rodríguez VM, Díaz-Urbano M, Sklenář F, Saati-Santamaría Z, et al. Endophytic fungi from kale (Brassica oleracea var. acephala) modify roots-glucosinolate profile and promote plant growth in cultivated Brassica species. First description of Pyrenophora gallaeciana. Front Microbiol. 2022;13:981507. doi: 10.3389/fmicb.2022.981507. PubMed DOI PMC
Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK. Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods. 2016;8:12–24. doi: 10.1039/C5AY02550H. DOI
Ranadev P, Revanna A, Bagyaraj DJ, Shinde AH. Sulfur oxidizing bacteria in agro ecosystem and its role in plant productivity—a review. J Appl Microbiol. 2023;134(8):lxad161. doi: 10.1093/jambio/lxad161. PubMed DOI
Rhuland LE, Work E, Denman RF, Hoare DS. The behaviour of the isomers of α, ε-diaminopimelic acid on paper chromatograms. J Am Chem Soc. 1995;77:4844–4846. doi: 10.1021/ja01623a047. DOI
Rodriguez-R LM, Konstantinidis KT. The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes. PeerJ. 2016;4:e1900v1. PubMed
Rogers JS, Swofford DL. A fast method for approximating maximum likelihoods of phylogenetic trees from nucleotide sequences. Syst Biol. 1998;47:77–89. doi: 10.1080/106351598261049. PubMed DOI
Saati-Santamaría Z. Global map of specialized metabolites encoded in prokaryotic plasmids. Microbiol Spectr. 2023;11(4):e01523–e1623. doi: 10.1128/spectrum.01523-23. PubMed DOI PMC
Saati-Santamaría Z, Peral-Aranega E, Velázquez E, Rivas R, García-Fraile P. Phylogenomic analyses of the genus Pseudomonas lead to the rearrangement of several species and the definition of new genera. Biology. 2021;10:782. doi: 10.3390/biology10080782. PubMed DOI PMC
Saati-Santamaría Z, Baroncelli R, Rivas R, García-Fraile P. Comparative genomics of the genus pseudomonas reveals host-and environment-specific evolution. Microbiol Spectr. 2022;10(6):e02370–e2422. doi: 10.1128/spectrum.02370-22. PubMed DOI PMC
Saati-Santamaría Z, Selem-Mojica N, Peral-Aranega E, Rivas R, García-Fraile P. Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products. Microb Genom. 2022;8(2):000758. PubMed PMC
Saitou N, Nei M. A neighbour-joining method: a new method for reconstructing phylogenetics trees. Mol Biol Evol. 1987;44:406–425. PubMed
Sasse M. Identification of bacteria by gas chromatography of cellular fatty acids, MIDI Technical Note 101. Newark: MIDI Inc; 1990.
Sasse J, Martinoia E, Northen T. Feed your friends: do plant exudates shape the root microbiome? Trends Plant Sci. 2018;23(1):25–41. doi: 10.1016/j.tplants.2017.09.003. PubMed DOI
Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI
Senghor B, Seck EH, Khelaifia S, Bassene H, Sokhna C, Fournier PE, Raoult D, Lagier JC. Description of 'Bacillus dakarensis' sp. nov, 'Bacillus sinesaloumensis' sp. nov, 'Gracilibacillus timonensis' sp. nov, 'Halobacillus massiliensis' sp. nov, 'Lentibacillus massiliensis' sp. nov, 'Oceanobacillus senegalensis' sp. nov, 'Oceanobacillus timonensis' sp. nov, 'Virgibacillus dakarensis' sp. nov. and 'Virgibacillus marseillensis' sp. nov, nine halophilic new species isolated from human stool. New Microb New Infect. 2017;17:45–51. doi: 10.1016/j.nmni.2017.01.010. PubMed DOI PMC
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–3212. doi: 10.1093/bioinformatics/btv351. PubMed DOI
Simonin M, Briand M, Chesneau G, Rochefort A, Marais C, Sarniguet A, Barret M. Seed microbiota revealed by a large-scale meta-analysis including 50 plant species. New Phytol. 2022;234(4):1448–1463. doi: 10.1111/nph.18037. PubMed DOI
Son JS, Hwang YJ, Lee SY, Ghim SY. Bacillus salidurans sp. nov, isolated from salt-accumulated pepper rhizospheric soil. Int J Syst Evol Microbiol. 2019;69:116–122. doi: 10.1099/ijsem.0.003110. PubMed DOI
Syberg-Olsen MJ, Garber AI, Keeling PJ, McCutcheon JP, Husnik F. Pseudofinder: detection of pseudogenes in prokaryotic genomes. Mol Biol Evol. 2022;39(7):153. doi: 10.1093/molbev/msac153. PubMed DOI PMC
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. The clustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997;24:4876–4882. doi: 10.1093/nar/25.24.4876. PubMed DOI PMC
Tindall BJ. Lipid composition of Halobacterium lacusprofundi. FEMS Microbiol Lett. 1990;66:199–202. doi: 10.1111/j.1574-6968.1990.tb03996.x. DOI
Weisburg WG, Barns SM, Pelletier DA, Lane DJ. 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol. 1991;173(2):697–703. doi: 10.1128/jb.173.2.697-703.1991. PubMed DOI PMC
Wiesmann CL, Wang NR, Zhang Y, Liu Z, Haney CH. Origins of symbiosis: shared mechanisms underlying microbial pathogenesis, commensalism and mutualism of plants and animals. FEMS Microbiol Rev. 2022;47(6):fuac048. doi: 10.1093/femsre/fuac048. PubMed DOI PMC
Zhu Q, Kosoy M, Dittmar K. HGTector: an automated method facilitating genome-wide discovery of putative horizontal gene transfers. BMC Genom. 2014;15:717. doi: 10.1186/1471-2164-15-717. PubMed DOI PMC