Abstract
Plasmids, circular DNA that exist and replicate outside of the host chromosome, have been important in the spread of non-essential genes as well as the rapid evolution of prokaryotes. Recent advances in environmental engineering have aimed to utilize the mobility of plasmids carrying degradative genes to disseminate them into the environment for cost-effective and environmentally friendly remediation of harmful contaminants. Here, we review the knowledge surrounding plasmid transfer and the conditions needed for successful transfer and expression of degradative plasmids. Both abiotic and biotic factors have a great impact on the success of degradative plasmid transfer and expression of the degradative genes of interest. Properties such as ecological growth strategies of bacteria may also contribute to plasmid transfer and may be an important consideration for bioremediation applications. Finally, the methods for detection of conjugation events have greatly improved and the application of these tools can help improve our understanding of conjugation in complex communities. However, it remains clear that more methods for in situ detection of plasmid transfer are needed to help detangle the complexities of conjugation in natural environments to better promote a framework for precision bioremediation.
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References
Alanis AJ (2005) Resistance to antibiotics: are we in the post-antibiotic era? Arch Med Res 36:697–705
Alderliesten JB, Duxbury SJN, Zwart MP et al (2020) Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis. BMC Microbiol. https://doi.org/10.1186/s12866-020-01825-4
Aminov RI (2011) Horizontal gene exchange in environmental microbiota. Front Microbiol 2:158
Andreoni V, Gianfreda L (2007) Bioremediation and monitoring of aromatic-polluted habitats. Appl Microbiol Biotechnol 76:287–308. https://doi.org/10.1007/s00253-007-1018-5
Atlas RM, Bartha R (1997) Microbial ecology: fundamentals and applications, 4th edn. Benjamin Cummings, San Francisco
Baltrus DA (2013) Exploring the costs of horizontal gene transfer. Trends Ecol Evol 28:489–495
Bergstrom CT, Lipsitch M, Levin BR (2000) Natural selection, infectious transfer and the existence conditions for bacterial plasmids. Genetics 155:1505–1519
Bleakley BH, Crawford DL (1989) The effect of varying moisture and nutrient levels on the transfer of a conjugative plasmid between Streptomyces species in soil Fungal Growth on Soil Substances View project. The potential effects of woodchip bioreactors on transporting microbes. Can J Microbiol. https://doi.org/10.1139/m89-086
Brzeszcz J, Steliga T, Kapusta P et al (2016) r-strategist versus K-strategist for the application in bioremediation of hydrocarbon-contaminated soils. Int Biodeterior Biodegrad 106:41–52. https://doi.org/10.1016/j.ibiod.2015.10.001
Cavalli LL, Lederberg J, Lederberg EM (1953) An infective factor controlling sex compatibility in Bacterium coli. J Gen Microbiol 8:89–103. https://doi.org/10.1099/00221287-8-1-89
César CE, Machón C, De La Cruz F, Llosa M (2006) A new domain of conjugative relaxase TrwC responsible for efficient oriT-specific recombination on minimal target sequences. Mol Microbiol 62:984–996. https://doi.org/10.1111/j.1365-2958.2006.05437.x
Christie PJ, Cascales E (2009) Structural and dynamic properties of bacterial Type IV secretion systems (Review). Mol Membr Biol 22:51–61. https://doi.org/10.1080/09687860500063316
Datta N, Hedges RW (1973) R factors of compatibility group A. J Gen Microbiol 74:335–337. https://doi.org/10.1099/00221287-74-2-335
De Gelder L, Ponciano JM, Joyce P, Top EM (2007) Stability of a promiscuous plasmid in different hosts: No guarantee for a long-term relationship. Microbiology 153:452–463. https://doi.org/10.1099/mic.0.2006/001784-0
DiGiovanni GD, Neilson JW, Pepper IL, Sinclair NA (1996) Gene transfer of Alcaligenes eutrophus JMP134 plasmid pJP4 to indigenous soil recipients. Appl Environ Microbiol 62:2521–2526. https://doi.org/10.1128/aem.62.7.2521-2526.1996
Draper O, César CE, Machón C et al (2005) Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc Natl Acad Sci USA 102:16385–16390. https://doi.org/10.1073/pnas.0506081102
Elsas JD, Bailey MJ (2006) The ecology of transfer of mobile genetic elements. FEMS Microbiol Ecol 42:187–197. https://doi.org/10.1111/j.1574-6941.2002.tb01008.x
Fernandez-Astorga A, Muela A, Cisterna R et al (1992) Biotic and abiotic factors affecting plasmid transfer in Escherichia coli strains. Appl Environ Microbiol 58:392–398
Fernandez-Lopez R, de Toro M, Moncalian G et al (2016) Comparative genomics of the conjugation region of F-like plasmids: five shades of F. Front Mol Biosci. https://doi.org/10.3389/fmolb.2016.00071
Fernandez-Lopez R, Redondo S, Garcillan-Barcia MP, de la Cruz F (2017) Towards a taxonomy of conjugative plasmids. Curr Opin Microbiol 38:106–113
Fierer N (2017) Embracing the unknown: disentangling the complexities of the soil microbiome. Nat Publ Gr. https://doi.org/10.1038/nrmicro.2017.87
Fierer N, Bradford MA, Jackson RB (2007) Toward an ecological classification of soil bacteria. Ecology 88:1354–1364. https://doi.org/10.1890/05-1839
Firth N, Ippen-ihler K, Skurray RA (1996) Structure and function of the F factor and mechanism of conjugation Escherichia coli Salmonella typhimurium. Cell Mol Biol 126:2377–2401
Forns N, Baños RC, Balsalobre C et al (2005) Temperature-dependent conjugative transfer of R27: role of chromosome-and plasmid-encoded Hha and H-NS proteins. J Bacteriol 187:3950–3959. https://doi.org/10.1128/JB.187.12.3950-3959.2005
Fox RE, Zhong X, Krone SM, Top EM (2008) Spatial structure and nutrients promote invasion of IncP-1 plasmids in bacterial populations. ISME J 2:1024–1039. https://doi.org/10.1038/ismej.2008.53
Fricke WF, Welch TJ, McDermott PF et al (2009) Comparative genomics of the IncA/C multidrug resistance plasmid family. J Bacteriol 191:4750–4757. https://doi.org/10.1128/JB.00189-09
Frost LS, Ippen-Ihler K, Skurray RA (1994) Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev 58:162–210
Frost LS, Leplae R, Summers AO, Toussaint A (2005) Mobile genetic elements: the agents of open source evolution. Nat Rev Microbiol 3:722–732
Furste JP, Pansegrau W, Ziegelin G et al (1989) Conjungative transfer of promiscuous IncP plasmids: interaction of plasmid-encoded products with the transfer origin. Proc Natl Acad Sci USA 86:1771–1775. https://doi.org/10.1073/pnas.86.6.1771
Gao C, Jin X, Ren J et al (2015) Bioaugmentation of DDT-contaminated soil by dissemination of the catabolic plasmid pDOD. J Environ Sci (china) 27:42–50. https://doi.org/10.1016/j.jes.2014.05.045
Garbisu C, Garaiyurrebaso O, Epelde L et al (2017) Plasmid-mediated bioaugmentation for the bioremediation of contaminated soils. Front Microbiol 8:1966. https://doi.org/10.3389/fmicb.2017.01966
Garcillán-Barcia MP, Jurado P, González-Pérez B et al (2007) Conjugative transfer can be inhibited by blocking relaxase activity within recipient cells with intrabodies. Mol Microbiol 63:404–416. https://doi.org/10.1111/j.1365-2958.2006.05523.x
Gogarten JP, Townsend JP (2005) Horizontal gene transfer, genome innovation and evolution. Nat Rev Microbiol 3:679–687
Grohmann E, Muth G, Espinosa M (2003) Conjugative plasmid transfer in Gram-positive bacteria. Microbiol Mol Biol Rev 67:277–301. https://doi.org/10.1128/mmbr.67.2.277-301.2003
Gullberg E, Albrecht LM, Karlsson C et al (2014) Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. Mbio. https://doi.org/10.1128/mBio.01918-14
Haase J, Lurz R, Grahn AM et al (1995) Bacterial conjugation mediated by plasmid RP4: RSF1010 mobilization, donor-specific phage propagation, and pilus production require the same Tra2 core components of a proposed DNA transport complex. J Bacteriol 177:4779–4791. https://doi.org/10.1128/jb.177.16.4779-4791.1995
Hall JPJ, Wood AJ, Harrison E, Brockhurst MA (2016) Source-sink plasmid transfer dynamics maintain gene mobility in soil bacterial communities. Proc Natl Acad Sci USA 113:8260–8265. https://doi.org/10.1073/pnas.1600974113
Harrison E, Guymer D, Spiers AJ et al (2015) Parallel compensatory evolution stabilizes plasmids across the parasitism-mutualism continuum. Curr Biol 25:2034–2039. https://doi.org/10.1016/j.cub.2015.06.024
Hayes F (2003) The function and organization of plasmids. Methods Mol Biol 235:1–17. https://doi.org/10.1385/1-59259-409-3:1
Headd B, Bradford SA (2018) Physicochemical factors that favor conjugation of an antibiotic resistant plasmid in non-growing bacterial cultures in the absence and presence of antibiotics. Front Microbiol 9:2122. https://doi.org/10.3389/fmicb.2018.02122
Ikuma K, Gunsch CK (2012) Genetic bioaugmentation as an effective method for in situ bioremediation: functionality of catabolic plasmids following conjugal transfers. Bioengineered 3:236–241. https://doi.org/10.4161/bbug.20551
Ikuma K, Gunsch CK (2013) Functionality of the TOL plasmid under varying environmental conditions following conjugal transfer. Appl Microbiol Biotechnol 97:395–408. https://doi.org/10.1007/s00253-012-3949-8
Ikuma K, Holzem RM, Gunsch CK (2012) Impacts of organic carbon availability and recipient bacteria characteristics on the potential for TOL plasmid genetic bioaugmentation in soil slurries. Chemosphere 89:158–163. https://doi.org/10.1016/j.chemosphere.2012.05.086
Johnsen AR, Kroer N (2007) Effects of stress and other environmental factors on horizontal plasmid transfer assessed by direct quantification of discrete transfer events. FEMS Microbiol Ecol 59:718–728. https://doi.org/10.1111/j.1574-6941.2006.00230.x
Kennedy N, Beutin L, Achtman M et al (1977) Conjugation proteins encoded by the F sex factor. Nature 270:580–585. https://doi.org/10.1038/270580a0
Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333. https://doi.org/10.1128/AEM.66.4.1328-1333.2000
Kottara A, Hall JPJ, Harrison E, Brockhurst MA (2018) Variable plasmid fitness effects and mobile genetic element dynamics across Pseudomonas species. FEMS Microbiol Ecol 94:172. https://doi.org/10.1093/femsec/fix172
Król JE, Nguyen HD, Rogers LM et al (2011) Increased transfer of a multidrug resistance plasmid in Escherichia coli biofilms at the air-liquid interface. Appl Environ Microbiol 77:5079–5088. https://doi.org/10.1128/AEM.00090-11
Kumar CC, Novick RP (1985) Plasmid pT181 replication is regulated by two countertranscripts. Proc Natl Acad Sci USA 82:638–642. https://doi.org/10.1073/pnas.82.3.638
Lafuente R, Maymó-Gatell X, Mas-Castellà J, Guerrero R (1996) Influence of environmental factors on plasmid transfer in soil microcosms. Curr Microbiol 32:213–220
Lanka E, Wilkins BM (1995) DNA processing reactions in bacterial conjugation. Annu Rev Biochem 64:141–169
Lawley TD, Klimke WA, Gubbins MJ, Frost LS (2003) F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 224:1–15
Li L, Dechesne A, Madsen JS et al (2020) Plasmids persist in a microbial community by providing fitness benefit to multiple phylotypes. ISME J 14:1170–1181. https://doi.org/10.1038/s41396-020-0596-4
Light J, Molin S (1982) The sites of action of the two copy number control functions of plasmid R1. MGG Mol Gen Genet 187:486–493. https://doi.org/10.1007/BF00332633
Lopatkin AJ, Meredith HR, Srimani JK et al (2017) Persistence and reversal of plasmid-mediated antibiotic resistance. Nat Commun. https://doi.org/10.1038/s41467-017-01532-1
MacLean RC, San Millan A (2015) Microbial evolution: towards resolving the plasmid paradox. Curr Biol 25:R764–R767
Megharaj M, Ramakrishnan B, Venkateswarlu K et al (2011) Bioremediation approaches for organic pollutants: a critical perspective. Environ Int. https://doi.org/10.1016/j.envint.2011.06.003
Miller MN, Stratton GW, Murray G (2004) Effects of soil moisture and aeration on the biodegradation of pentachlorophenol contaminated soil. Bull Environ Contam Toxicol 72:101–108. https://doi.org/10.1007/s00128-003-0246-3
Mrozik A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165:363–375. https://doi.org/10.1016/j.micres.2009.08.001
Mulligan ME, Mcclure WR (1986) Analysis of the occurrence of promoter-sites in DNA. Nucleic Acids Res 14:109–126. https://doi.org/10.1093/nar/14.1.109
Navarre WW, McClelland M, Libby SJ, Fang FC (2007) Silencing of xenogeneic DNA by H-NS - Facilitation of lateral gene transfer in bacteria by a defense system that recognizes foreign DNA. Genes Dev 21:1456–1471
Navarre WW, Porwollik S, Wang Y et al (2006) Selective silencing of foreign DNA with low GC content by the H-NS protein in Salmonella. Science 313:236–238. https://doi.org/10.1126/science.1128794
Novick RP (1987) Plasmid incompatibility. Microbiol Rev 51:381–395
Novick RP, Hoppensteadt FC (1978) On plasmid incompatibility. Plasmid 1:421–434. https://doi.org/10.1016/0147-619X(78)90001-X
O’Brien TF (2002) Emergence, spread, and environmental effect of antimicrobial resistance: how use of an antimicrobial anywhere can increase resistance to any antimicrobial anywhere else. Clin Infect Dis 34:S78–S84. https://doi.org/10.1086/340244
Ortiz-Álvarez R et al (2018) Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J. https://doi.org/10.1038/s41396-018-0076-2
Pearce DA, Bazin MJ, Lynch JM (2008) Substrate concentration and plasmid transfer frequency between bacteria in a model rhizosphere. Microbiol Ecol 40:2357–2368. https://doi.org/10.1016/B978-008045405-4.00519-X
Pinedo CA, Smets BF (2005) Conjugal TOL transfer from Pseudomonas putida to Pseudomonas aeruginosa: effects of restriction proficiency, toxicant exposure, cell density ratios, and conjugation detection method on observed transfer efficiencies. Appl Environ Microbiol 71:51–57. https://doi.org/10.1128/AEM.71.1.51-57.2005
Popa O, Hazkani-Covo E, Landan G et al (2011) Directed networks reveal genomic barriers and DNA repair bypasses to lateral gene transfer among prokaryotes. Genome Res 21:599–609. https://doi.org/10.1101/gr.115592.110
Roller BRK, Stoddard SF, Schmidt TM (2016) Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat Microbiol 1:1–7. https://doi.org/10.1038/nmicrobiol.2016.160
San Millan A, Toll-Riera M, Qi Q et al (2018) Integrative analysis of fitness and metabolic effects of plasmids in Pseudomonas aeruginosa PAO1. ISME J 12:3014–3024. https://doi.org/10.1038/s41396-018-0224-8
Santos SR, Ochman H (2004) Identification and phylogenetic sorting of bacterial lineages with universally conserved genes and proteins. Environ Microbiol 6:754–759. https://doi.org/10.1111/j.1462-2920.2004.00617.x
Seoane J, Yankelevich T, Dechesne A et al (2010) An individual-based approach to explain plasmid invasion in bacterial populations. FEMS Microbiol Ecol 75:17–27. https://doi.org/10.1111/j.1574-6941.2010.00994.x
Shachrai I, Zaslaver A, Alon U, Dekel E (2010) Cost of unneeded proteins in E. coli is reduced after several generations in exponential growth. Mol Cell 38:758–767. https://doi.org/10.1016/j.molcel.2010.04.015
Shintani M, Matsui K, Takemura T et al (2008) Behavior of the IncP-7 carbazole-degradative plasmid pCAR1 in artificial environmental samples. Appl Microbiol Biotechnol 80:485–497. https://doi.org/10.1007/s00253-008-1564-5
Simonsen L (2018) The existence conditions for bacterial plasmids: theory and reality. Microbiol Ecol 22:187–205
Smets BF, Rittmann BE, Stahl DA (1993a) The specific growth rate of Pseudomonas putida PAW1 influences the conjugal transfer rate of the TOL plasmid. Appl Environ Microbiol 59:3430–3437. https://doi.org/10.1128/aem.59.10.3430-3437.1993
Sørensen SJ, Bailey M, Hansen LH et al (2005) Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3:700–710. https://doi.org/10.1038/nrmicro1232
Stalder T, Top E (2016) Plasmid Transfer in biofilms: a perspective on limitations and opportunities. NPJ Biofilms Microbiomes. https://doi.org/10.1038/npjbiofilms.2016.22
Svara F, Rankin DJ (2011) The evolution of plasmid-carried antibiotic resistance. BMC Evol Biol 11:130. https://doi.org/10.1186/1471-2148-11-130
Sysoeva TA, Kim Y, Rodriguez J et al (2019) Growth-stage-dependent regulation of conjugation. AIChE J 66:1–10. https://doi.org/10.1002/aic.16848
Thomas CM, Nielsen KM (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3:711–721. https://doi.org/10.1038/nrmicro1234
Thompson IP, Van Der Gast CJ, Ciric L, Singer AC (2005) Bioaugmentation for bioremediation: the challenge of strain selection. Environ Microbiol 7:909–915
Tomizawa J, Itoh T, Selzer G, Som T (1981) Inhibition of ColE1 RNA primer formation by a plasmid-specified small RNA. Proc Natl Acad Sci USA 78:1421–1425. https://doi.org/10.1073/pnas.78.3.1421
Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14:262–269. https://doi.org/10.1016/S0958-1669(03)00066-1
Top EM, Springael D, Boon N (2002) Catabolic mobile genetic elements and their potential use in bioaugmentation of polluted soils and waters. FEMS Microbiol Ecol 42:199–208. https://doi.org/10.1111/j.1574-6941.2002.tb01009.x
Venkata Mohan S, Falkentoft C, Venkata Nancharaiah Y et al (2009) Bioaugmentation of microbial communities in laboratory and pilot scale sequencing batch biofilm reactors using the TOL plasmid. Bioresour Technol 100:1746–1753. https://doi.org/10.1016/j.biortech.2008.09.048
Vieira-Silva S, Rocha EPC (2010) The systemic imprint of growth and its uses in ecological (meta)genomics. PLoS Genet. https://doi.org/10.1371/journal.pgen.1000808
Vogwill T, Maclean RC (2015) The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach. Evol Appl 8:284–295. https://doi.org/10.1111/eva.12202
Von Wintersdorff CJH, Penders J, Van Niekerk JM et al (2016) Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer. Front Microbiol 7:173
Wang Y, Kou S, Jiang Q et al (2014) Factors affecting transfer of degradative plasmids between bacteria in soils. Appl Soil Ecol 84:254–261. https://doi.org/10.1016/j.apsoil.2014.07.009
Wickham SA, Lynn DH (1990) Relations between growth rate, cell size, and DNA content in colpodean ciliates (Ciliophora: Colpodea). Eur J Protistol 25:345–352. https://doi.org/10.1016/S0932-4739(11)80127-6
Wu L, Yang Y, Chen S et al (2017) Microbial functional trait of rRNA operon copy numbers increases with organic levels in anaerobic digesters. ISME J 11:2874–2878. https://doi.org/10.1038/ismej.2017.135
Zhang Q, Wang B, Cao Z, Yu Y (2012) Plasmid-mediated bioaugmentation for the degradation of chlorpyrifos in soil. J Hazard Mater 221–222:178–184. https://doi.org/10.1016/j.jhazmat.2012.04.024
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This work is supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE-1644868 and the National Institute of Health under grant no. P42ES010356.
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This work is supported by the National Science Foundation Graduate Research Fellowship under grant no. DGE-1644868 and the National Institute of Health under grant no. P42ES010356.
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Varner, P.M., Gunsch, C.K. Properties affecting transfer and expression of degradative plasmids for the purpose of bioremediation. Biodegradation 32, 361–375 (2021). https://doi.org/10.1007/s10532-021-09950-1
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DOI: https://doi.org/10.1007/s10532-021-09950-1