Global Map of Specialized Metabolites Encoded in Prokaryotic Plasmids

. 2023 Aug 17 ; 11 (4) : e0152323. [epub] 20230613

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37310275

Plasmids are the main mobile elements responsible for horizontal gene transfer (HGT) in microorganisms. These replicons extend the metabolic spectrum of their host cells by carrying functional genes. However, it is still unknown to what extent plasmids carry biosynthetic gene clusters (BGCs) related to the production of secondary or specialized metabolites (SMs). Here, we analyzed 9,183 microbial plasmids to unveil their potential to produce SMs, finding a large diversity of cryptic BGCs in a few varieties of prokaryotic host taxa. Some of these plasmids harbored 15 or more BGCs, and many others were exclusively dedicated to mobilizing BGCs. We found an occurrence pattern of BGCs within groups of homologous plasmids shared by a common taxon, mainly in host-associated microbes (e.g., Rhizobiales, Enterobacteriaceae members). Our results add to the knowledge of the ecological functions and potential industrial uses of plasmids and shed light on the dynamics and evolution of SMs in prokaryotes. IMPORTANCE Plasmids are mobile DNA elements that can be shared among microbial cells, and they are useful for bringing to fruition some microbial ecological traits. However, it is not known to what extent plasmids harbor genes related to the production of specialized/secondary metabolites (SMs). In microbes, these metabolites are frequently useful for defense purposes, signaling, etc. In addition, these molecules usually have biotechnological and clinical applications. Here, we analyzed the content, dynamics, and evolution of genes related to the production of SMs in >9,000 microbial plasmids. Our results confirm that some plasmids act as a reservoir of SMs. We also found that some families of biosynthetic gene clusters are exclusively present in some groups of plasmids shared among closely related microbes. Host-associated bacteria (e.g., plant and human microbes) harbor the majority of specialized metabolites encoded in plasmids. These results provide new knowledge about microbial ecological traits and might enable the discovery of novel metabolites.

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Atanasov AG, Zotchev SB, Dirsch VM, Supuran CT, International Natural Product Sciences Taskforce . 2021. Natural products in drug discovery: advances and opportunities. Nat Rev Drug Discov 20:200–216. doi:10.1038/s41573-020-00114-z. PubMed DOI PMC

Hemmerling F, Piel J. 2022. Strategies to access biosynthetic novelty in bacterial genomes for drug discovery. Nat Rev Drug Discov 21:359–378. doi:10.1038/s41573-022-00414-6. PubMed DOI

Yang R, Shi Q, Huang T, Yan Y, Li S, Fang Y, Li Y, Liu L, Liu L, Wang X, Peng Y, Fan J, Zou L, Lin S, Chen G. 2023. The natural pyrazolotriazine pseudoiodinine from Pseudomonas mosselii 923 inhibits plant bacterial and fungal pathogens. Nat Commun 14:734. doi:10.1038/s41467-023-36433-z. PubMed DOI PMC

Davies J. 2013. Specialized microbial metabolites: functions and origins. J Antibiot (Tokyo) 66:361–364. doi:10.1038/ja.2013.61. PubMed DOI

Chevrette MG, Gutiérrez-García K, Selem-Mojica N, Aguilar-Martínez C, Yañez-Olvera A, Ramos-Aboites HE, Hoskisson PA, Barona-Gómez F. 2020. Evolutionary dynamics of natural product biosynthesis in bacteria. Nat Prod Rep 37:566–599. doi:10.1039/c9np00048h. PubMed DOI

Gavriilidou A, Kautsar SA, Zaburannyi N, Krug D, Müller R, Medema MH, Ziemert N. 2022. Compendium of specialized metabolite biosynthetic diversity encoded in bacterial genomes. Nat Microbiol 7:726–735. doi:10.1038/s41564-022-01110-2. PubMed DOI

Zan J, Li Z, Tianero MD, Davis J, Hill RT, Donia MS. 2019. A microbial factory for defensive kahalalides in a tripartite marine symbiosis. Science 364:eaaw6732. doi:10.1126/science.aaw6732. PubMed DOI

Essarioui A, LeBlanc N, Otto-Hanson L, Schlatter DC, Kistler HC, Kinkel LL. 2020. Inhibitory and nutrient use phenotypes among coexisting Fusarium and Streptomyces populations suggest local coevolutionary interactions in soil. Environ Microbiol 22:976–985. doi:10.1111/1462-2920.14782. PubMed DOI

Chevrette MG, Handelsman J. 2021. Needles in haystacks: reevaluating old paradigms for the discovery of bacterial secondary metabolites. Nat Prod Rep 38:2083–2099. doi:10.1039/d1np00044f. PubMed DOI

Fukuda TTH, Helfrich EJN, Mevers E, Melo WGP, Van Arnam EB, Andes DR, Currie CR, Pupo MT, Clardy J. 2021. Specialized metabolites reveal evolutionary history and geographic dispersion of a multilateral symbiosis. ACS Cent Sci 7:292–299. doi:10.1021/acscentsci.0c00978. PubMed DOI PMC

Vicente I, Baroncelli R, Hermosa R, Monte E, Vannacci G, Sarrocco S. 2022. Role and genetic basis of specialised secondary metabolites in Trichoderma ecophysiology. Fungal Biol Rev 39:83–99. doi:10.1016/j.fbr.2021.12.004. DOI

Saati-Santamaría Z, Baroncelli R, Rivas R, García-Fraile P. 2022. Comparative genomics of the genus Pseudomonas reveals host- and environment-specific evolution. Microbiol Spectr 10:e02370-22. doi:10.1128/spectrum.02370-22. PubMed DOI PMC

Wang X, Jarmusch SA, Frisvad JC, Larsen TO. 2023. Current status of secondary metabolite pathways linked to their related biosynthetic gene clusters in Aspergillus section Nigri. Nat Prod Rep 40:237–274. doi:10.1039/D1NP00074H. PubMed DOI

Saati-Santamaría Z, Selem-Mojica N, Peral-Aranega E, Rivas R, García-Fraile P. 2022. Unveiling the genomic potential of Pseudomonas type strains for discovering new natural products. Microb Genom 8:000758. doi:10.1099/mgen.0.000758. PubMed DOI PMC

Navarro-Muñoz JC, Selem-Mojica N, Mullowney MW, Kautsar SA, Tryon JH, Parkinson EI, De Los Santos ELC, Yeong M, Cruz-Morales P, Abubucker S, Roeters A, Lokhorst W, Fernandez-Guerra A, Cappelini LTD, Goering AW, Thomson RJ, Metcalf WW, Kelleher NL, Barona-Gomez F, Medema MH. 2020. A computational framework to explore large-scale biosynthetic diversity. Nat Chem Biol 16:60–68. doi:10.1038/s41589-019-0400-9. PubMed DOI PMC

Brooks L, Kaze M, Sistrom M. 2019. A curated, comprehensive database of plasmid sequences. Microbiol Resour Announc 8:e01325-18. doi:10.1128/MRA.01325-18. PubMed DOI PMC

Redondo-Salvo S, Fernández-López R, Ruiz R, Vielva L, de Toro M, Rocha EPC, Garcillán-Barcia MP, de la Cruz F. 2020. Pathways for horizontal gene transfer in bacteria revealed by a global map of their plasmids. Nat Commun 11:3602. doi:10.1038/s41467-020-17278-2. PubMed DOI PMC

Schmartz GP, Hartung A, Hirsch P, Kern F, Fehlmann T, Müller R, Keller A. 2022. PLSDB: advancing a comprehensive database of bacterial plasmids. Nucleic Acids Res 50:D273–D278. doi:10.1093/nar/gkab1111. PubMed DOI PMC

Wick RR, Judd LM, Wyres KL, Holt KE. 2021. Recovery of small plasmid sequences via Oxford Nanopore sequencing. Microb Genom 7:000631. doi:10.1099/mgen.0.000631. PubMed DOI PMC

Dai D, Brown C, Bürgmann H, Larsson DGJ, Nambi I, Zhang T, Flach C-F, Pruden A, Vikesland PJ. 2022. Long-read metagenomic sequencing reveals shifts in associations of antibiotic resistance genes with mobile genetic elements from sewage to activated sludge. Microbiome 10:20. doi:10.1186/s40168-021-01216-5. PubMed DOI PMC

Rodríguez-Beltrán J, DelaFuente J, Leon-Sampedro R, MacLean RC, San Millan A. 2021. Beyond horizontal gene transfer: the role of plasmids in bacterial evolution. Nat Rev Microbiol 19:347–359. doi:10.1038/s41579-020-00497-1. PubMed DOI

Wright RC, Brockhurst MA. 2022. Plasmid evolution in the clinic. Nat Ecol Evol 6:1806–1807. doi:10.1038/s41559-022-01907-8. PubMed DOI

Reid CJ, Cummins ML, Börjesson S, Brouwer MSM, Hasman H, Hammerum AM, Roer L, Hess S, Berendonk T, Nešporová K, Haenni M, Madec J-Y, Bethe A, Michael GB, Schink A-K, Schwarz S, Dolejska M, Djordjevic SP. 2022. A role for ColV plasmids in the evolution of pathogenic Escherichia coli ST58. Nat Commun 13:683. doi:10.1038/s41467-022-28342-4. PubMed DOI PMC

Arashida H, Odake H, Sugawara M, Noda R, Kakizaki K, Ohkubo S, Mitsui H, Sato S, Minamisawa K. 2022. Evolution of rhizobial symbiosis islands through insertion sequence-mediated deletion and duplication. ISME J 16:112–121. doi:10.1038/s41396-021-01035-4. PubMed DOI PMC

Brinkmann H, Göker M, Koblížek M, Wagner-Döbler I, Petersen J. 2018. Horizontal operon transfer, plasmids, and the evolution of photosynthesis in Rhodobacteraceae. ISME J 12:1994–2010. doi:10.1038/s41396-018-0150-9. PubMed DOI PMC

Mochizuki S, Hiratsu K, Suwa M, Ishii T, Sugino F, Yamada K, Kinashi H. 2003. The large linear plasmid pSLA2-L of Streptomyces rochei has an unusually condensed gene organization for secondary metabolism. Mol Microbiol 48:1501–1510. doi:10.1046/j.1365-2958.2003.03523.x. PubMed DOI

Medema MH, Trefzer A, Kovalchuk A, van den Berg M, Müller U, Heijne W, Wu L, Alam MT, Ronning CM, Nierman WC, Bovenberg RAL, Breitling R, Takano E. 2010. The sequence of a 1.8-Mb bacterial linear plasmid reveals a rich evolutionary reservoir of secondary metabolic pathways. Genome Biol Evol 2:212–224. doi:10.1093/gbe/evq013. PubMed DOI PMC

Slemc L, Jakše J, Filisetti A, Baranasic D, Rodríguez-García A, Del Carratore F, Marino SM, Zucko J, Starcevic A, Šala M, Pérez-Bonilla M, Sánchez-Hidalgo M, González I, Reyes F, Genilloud O, Springthorpe V, Goranovič D, Kosec G, Thomas GH, Lucrezia DD, Petković H, Tome M. 2022. Reference-grade genome and large linear plasmid of Streptomyces rimosus: pushing the limits of Nanopore sequencing. Microbiol Spectr 10:e02434-21. doi:10.1128/spectrum.02434-21. PubMed DOI PMC

Pilosof S. 2023. Conceptualizing microbe-plasmid communities as complex adaptive systems. Trends Microbiol doi:10.1016/j.tim.2023.01.007. PubMed DOI

Keller NP. 2019. Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol 17:167–180. doi:10.1038/s41579-018-0121-1. PubMed DOI PMC

Menéndez E, García-Fraile P. 2017. Plant probiotic bacteria: solutions to feed the world. AIMS Microbiol 3:502–524. doi:10.3934/microbiol.2017.3.502. PubMed DOI PMC

diCenzo GC, Tesi M, Pfau T, Mengoni A, Fondi M. 2020. Genome-scale metabolic reconstruction of the symbiosis between a leguminous plant and a nitrogen-fixing bacterium. Nat Commun 11:2574. doi:10.1038/s41467-020-16484-2. PubMed DOI PMC

Shiner EK, Rumbaugh KP, Williams SC. 2005. Interkingdom signaling: deciphering the language of acyl homoserine lactones. FEMS Microbiol Rev 29:935–947. doi:10.1016/j.femsre.2005.03.001. PubMed DOI

Ji Y-Y, Zhang B, Zhang P, Chen L-C, Si Y-W, Wan X-Y, Li C, Wang R-H, Tian Y, Zhang Z, Tian C-F. 2023. Rhizobial migration toward roots mediated by FadL-ExoFQP modulation of extracellular long-chain AHLs. ISME J 17:417–431. doi:10.1038/s41396-023-01357-5. PubMed DOI PMC

Smith LT, Allaith AA, Smith GM. 1994. Mechanism of osmotically regulated N-acetylglutaminylglutamine amide production in Rhizobium meliloti. Plant Soil 161:103–108. doi:10.1007/BF02183090. DOI

Kurz M, Burch AY, Seip B, Lindow SE, Gross H. 2010. Genome-driven investigation of compatible solute biosynthesis pathways of Pseudomonas syringae pv. syringae and their contribution to water stress tolerance. Appl Environ Microbiol 76:5452–5462. doi:10.1128/AEM.00686-10. PubMed DOI PMC

Velásquez AC, Huguet-Tapia JC, He SY. 2022. Shared in planta population and transcriptomic features of nonpathogenic members of endophytic phyllosphere microbiota. Proc Natl Acad Sci USA 119:e2114460119. doi:10.1073/pnas.2114460119. PubMed DOI PMC

Loper JE, Buyer JS. 1991. Siderophores in microbial interactions on plant surfaces. MPMI 4:5–13. doi:10.1094/MPMI-4-005. DOI

Gu S, Wei Z, Shao Z, Friman V-P, Cao K, Yang T, Kramer J, Wang X, Li M, Mei X, Xu Y, Shen Q, Kümmerli R, Jousset A. 2020. Competition for iron drives phytopathogen control by natural rhizosphere microbiomes. Nat Microbiol 5:1002–1010. doi:10.1038/s41564-020-0719-8. PubMed DOI PMC

Mahajan SG, Nandre VS, Kodam KM, Kulkarni MV. 2021. Desferrioxamine E produced by an indigenous salt tolerant Pseudomonas stutzeri stimulates iron uptake of Triticum aestivum L. Biocatal Agric Biotechnol 35:102057. doi:10.1016/j.bcab.2021.102057. DOI

Heemstra JR, Jr, Walsh CT, Sattely ES. 2009. Enzymatic tailoring of ornithine in the biosynthesis of the Rhizobium cyclic trihydroxamate siderophore vicibactinJ. J Am Chem Soc 131:15317–15329. doi:10.1021/ja9056008. PubMed DOI PMC

González V, Santamaría RI, Bustos P, Hernández-González I, Medrano-Soto A, Moreno-Hagelsieb G, Janga SC, Ramírez MA, Jiménez-Jacinto V, Collado-Vides J, Dávila G. 2006. The partitioned Rhizobium etli genome: genetic and metabolic redundancy in seven interacting replicons. Proc Natl Acad Sci USA 103:3834–3839. doi:10.1073/pnas.0508502103. PubMed DOI PMC

Takase S, Kurokawa R, Kondoh Y, Honda K, Suzuki T, Kawahara T, Ikeda H, Dohmae N, Osada H, Shin-Ya K, Kushiro T, Yoshida M, Matsumoto K. 2019. Mechanism of action of prethioviridamide, an anticancer ribosomally synthesized and post-translationally modified peptide with a polythioamide structure. ACS Chem Biol 14:1819–1828. doi:10.1021/acschembio.9b00410. PubMed DOI

Eyles TH, Vior NM, Lacret R, Truman AW. 2021. Understanding thioamitide biosynthesis using pathway engineering and untargeted metabolomics. Chem Sci 12:7138–7150. doi:10.1039/d0sc06835g. PubMed DOI PMC

Tan X, Qiu H, Li F, Cheng D, Zheng X, Wang B, Huang M, Li W, Li Y, Sang K, Song B, Du J, Chen H, Xie C. 2019. Complete genome sequence of sequevar 14M Ralstonia solanacearum strain HA4-1 reveals novel type III effectors acquired through horizontal gene transfer. Front Microbiol 10:1893. doi:10.3389/fmicb.2019.01893. PubMed DOI PMC

Gao Q, Wang X, Xu H, Xu Y, Ling J, Zhang D, Gao S, Liu X. 2012. Roles of iron acquisition systems in virulence of extraintestinal pathogenic Escherichia coli: salmochelin and aerobactin contribute more to virulence than heme in a chicken infection model. BMC Microbiol 12:143. doi:10.1186/1471-2180-12-143. PubMed DOI PMC

Murdoch CC, Skaar EP. 2022. Nutritional immunity: the battle for nutrient metals at the host–pathogen interface. Nat Rev Microbiol 20:657–670. doi:10.1038/s41579-022-00745-6. PubMed DOI PMC

Ongpipattanakul C, Desormeaux EK, DiCaprio A, Van Der Donk WA, Mitchell DA, Nair SK. 2022. Mechanism of action of ribosomally synthesized and post-translationally modified peptides. Chem Rev 122:14722–14814. doi:10.1021/acs.chemrev.2c00210. PubMed DOI PMC

Wang S, Lin S, Fang Q, Gyampoh R, Lu Z, Gao Y, Clarke DJ, Wu K, Trembleau L, Yu Y, Kyeremeh K, Milne BF, Tabudravu J, Deng H. 2022. Ribosomally synthesised and post-translationally modified peptide containing a β-enamino acid and a macrocyclic motif. Nat Commun 13:5044. doi:10.1038/s41467-022-32774-3. PubMed DOI PMC

Steinke K, Mohite OS, Weber T, Kovács ÁT. 2021. Phylogenetic distribution of secondary metabolites in the Bacillus subtilis species complex. mSystems 6:e00057-21. doi:10.1128/mSystems.00057-21. PubMed DOI PMC

Belknap KC, Park CJ, Barth BM, Andam CP. 2020. Genome mining of biosynthetic and chemotherapeutic gene clusters in Streptomyces bacteria. Sci Rep 10:2003. doi:10.1038/s41598-020-58904-9. PubMed DOI PMC

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

Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T. 2021. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res 49:W29–W35. doi:10.1093/nar/gkab335. PubMed DOI PMC

Terlouw BR, Blin K, Navarro-Muñoz JC, Avalon NE, Chevrette MG, Egbert S, Lee S, Meijer D, Recchia MJJ, Reitz ZL, van Santen JA, Selem-Mojica N, Tørring T, Zaroubi L, Alanjary M, Aleti G, Aguilar C, Al-Salihi SAA, Augustijn HE, Avelar-Rivas JA, Avitia-Domínguez LA, Barona-Gómez F, Bernaldo-Agüero J, Bielinski VA, Biermann F, Booth TJ, Carrion Bravo VJ, Castelo-Branco R, Chagas FO, Cruz-Morales P, Du C, Duncan KR, Gavriilidou A, Gayrard D, Gutiérrez-García K, Haslinger K, Helfrich EJN, van der Hooft JJJ, Jati AP, Kalkreuter E, Kalyvas N, Kang KB, Kautsar S, Kim W, Kunjapur AM, Li Y-X, Lin G-M, Loureiro C, Louwen JJR, Louwen NLL, et al.. 2023. MIBiG 3.0: a community-driven effort to annotate experimentally validated biosynthetic gene clusters. Nucleic Acids Res 51:D603–D610. doi:10.1093/nar/gkac1049. PubMed DOI PMC

Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. doi:10.1101/gr.1239303. PubMed DOI PMC

Wickham H. 2011. ggplot2. Wiley Interdiscip Rev Comput Stat 3:180–185. doi:10.1002/wics.147. DOI

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