Life Within a Contaminated Niche: Comparative Genomic Analyses of an Integrative Conjugative Element ICEnahCSV86 and Two Genomic Islands From Pseudomonas bharatica CSV86T Suggest Probable Role in Colonization and Adaptation

Frontiers in Microbiology - Tập 13
Balaram Mohapatra1, Harshit Malhotra1, Prashant S. Phale1
1Department of Biosciences and Bioengineering, Indian Institute of Technology Bombay, Mumbai, India

Tóm tắt

Comparative genomic and functional analyses revealed the presence of three genomic islands (GIs, >50 Kb size): ICEnahCSV86, Pseudomonas bharatica genomic island-1 (PBGI-1), and PBGI-2 in the preferentially aromatic-degrading soil bacterium, Pseudomonas bharatica CSV86T. Site-specific genomic integration at or near specific transfer RNAs (tRNAs), near-syntenic structural modules, and phylogenetic relatedness indicated their evolutionary lineage to the type-4 secretion system (T4SS) ICEclc family, thus predicting these elements to be integrative conjugative elements (ICEs). These GIs were found to be present as a single copy in the genome and the encoded phenotypic traits were found to be stable, even in the absence of selection pressure. ICEnahCSV86 harbors naphthalene catabolic (nah-sal) cluster, while PBGI-1 harbors Co-Zn-Cd (czc) efflux genes as cargo modules, whereas PBGI-2 was attributed to as a mixed-function element. The ICEnahCSV86 has been reported to be conjugatively transferred (frequency of 7 × 10–8/donor cell) to Stenotrophomonas maltophilia CSV89. Genome-wide comparative analyses of aromatic-degrading bacteria revealed nah-sal clusters from several Pseudomonas spp. as part of probable ICEs, syntenic to conjugatively transferable ICEnahCSV86 of strain CSV86T, suggesting it to be a prototypical element for naphthalene degradation. It was observed that the plasmids harboring nah-sal clusters were phylogenetically incongruent with predicted ICEs, suggesting genetic divergence of naphthalene metabolic clusters in the Pseudomonas population. Gene synteny, divergence estimates, and codon-based Z-test indicated that ICEnahCSV86 is probably derived from PBGI-2, while multiple recombination events masked the ancestral lineage of PBGI-1. Diversifying selection pressure (dN-dS = 2.27–4.31) imposed by aromatics and heavy metals implied the modular exchange-fusion of various cargo clusters through events like recombination, rearrangement, domain reshuffling, and active site optimization, thus allowing the strain to evolve, adapt, and maximize the metabolic efficiency in a contaminated niche. The promoters (Pnah and Psal) of naphthalene cargo modules (nah, sal) on ICEnahCSV86 were proved to be efficient for heterologous protein expression in Escherichia coli. GI-based genomic plasticity expands the metabolic spectrum and versatility of CSV86T, rendering efficient adaptation to the contaminated niche. Such isolate(s) are of utmost importance for their application in bioremediation and are the probable ideal host(s) for metabolic engineering.

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Tài liệu tham khảo

Arciszewska, 1991, Interaction of the Tn7-encoded transposition protein TnsB with the ends of the transposon., Nucleic Acids Res., 19, 5021, 10.1093/nar/19.18.5021

Badhai, 2016, Characterization of three novel SXT/R391 integrating conjugative elements ICEMfuInd1a and ICEMfuInd1b, and ICEMprChn1 identified in the genomes of Marinomonas fungiae JCM 18476T and Marinomonas profundimaris strain D104., Front. Microbiol., 7, 10.3389/fmicb.2016.01896

Baharoglu, 2013, Multiple pathways of genome plasticity leading to development of antibiotic resistance., Antibiotics, 2, 288, 10.3390/antibiotics2020288

Basu, 2006, Preferential utilization of aromatic compounds over glucose by Pseudomonas putida CSV86., Appl. Environ. Microbiol., 72, 2226, 10.1128/AEM.72.3.2226-2230.2006

Basu, 2003, Metabolism of benzyl alcohol via catechol ortho-pathway in methylnaphthalene-degrading Pseudomonas putida CSV86., Appl. Microbiol. Biotechnol., 62, 579, 10.1007/s00253-003-1305-8

Basu, 2008, Conjugative transfer of preferential utilization of aromatic compounds from Pseudomonas putida CSV86., Biodegradation, 19, 83, 10.1007/s10532-007-9117-7

Battle, 2009, Genomic islands of Pseudomonas aeruginosa., FEMS Microbiol. Lett., 290, 70, 10.1111/j.1574-6968.2008.01406.x

Bignell, 2001, The bacterial ParA-ParB partitioning proteins., J. Biotechnol., 91, 1, 10.1016/S0168-1656(01)00293-0

Bohlin, 2010, Analysis of intra-genomic GC content homogeneity within prokaryotes., BMC Genomics, 11, 10.1186/1471-2164-11-464

Bosch, 1999, Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10., Gene, 236, 149, 10.1016/s0378-1119(99)00241-3

Botelho, 2018, Unravelling the genome of a Pseudomonas aeruginosa isolate belonging to the high-risk clone ST235 reveals an integrative conjugative element housing a blaGES–6 carbapenemase., J. Antimicrob. Chemother., 73, 77, 10.1093/jac/dkx337

Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding., Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3

Burlage, 1990, Monitoring of naphthalene catabolism by bioluminescence with nah-lux transcriptional fusions., J. Bacteriol., 172, 4749, 10.1128/jb.172.9.4749-4757.1990

Burrus, 2017, Mechanisms of stabilization of integrative and conjugative elements., Curr. Opin. Microbiol., 38, 44, 10.1016/j.mib.2017.03.014

Burrus, 2002, Conjugative transposons: the tip of the iceberg., Mol. Microbiol., 46, 601, 10.1046/j.1365-2958.2002.03191.x

Calero, 2016, Broad-host-range ProUSER vectors enable fast characterization of inducible promoters and optimization of p-coumaric acid production in Pseudomonas putida KT2440., ACS Synth. Biol., 5, 741, 10.1021/acssynbio.6b00081

Chain, 2006, Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility., Proc. Natl. Acad. Sci. U.S.A., 103, 15280, 10.1073/pnas.0606924103

Christie, 2014, Mechanism and structure of the bacterial type IV secretion systems., Biochim. Biophys. Acta. Mol. Cell Res., 1843, 1578, 10.1016/j.bbamcr.2013.12.019

de Lorenzo, 1993, Analysis of Pseudomonas gene products using lacIq/Ptrp-lac plasmids and transposons that confer conditional phenotypes., Gene, 123, 17, 10.1016/0378-1119(93)90533-9

Delavat, 2017, The hidden life of integrative and conjugative elements., FEMS Microbiol. Rev., 41, 512, 10.1093/femsre/fux008

Dobrindt, 2004, Genomic islands in pathogenic and environmental microorganisms., Nat. Rev. Microbiol., 2, 414, 10.1038/nrmicro884

Duttagupta, 2020, Wide exposure of persistent organic pollutants (PoPs) in natural waters and sediments of the densely populated Western Bengal basin, India., Sci. Total Environ., 717, 10.1016/j.scitotenv.2020.137187

Eaton, 1994, Organization and evolution of naphthalene catabolic pathways: sequence of the DNA encoding 2-hydroxychromene-2-carboxylate isomerase and trans-o-hydroxybenzylidenepyruvate hydratase-aldolase from the NAH7 plasmid., J. Bacteriol., 176, 7757, 10.1128/jb.176.24.7757-7762.1994

Fang, 2010, Getting started in gene orthology and functional analysis., PLoS Comput. Biol., 6, 10.1371/journal.pcbi.1000703

Fuentes, 2014, Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications., Appl. Microbiol. Biotechnol., 98, 4781, 10.1007/s00253-014-5684-9

Gaillard, 2006, The clc element of Pseudomonas sp. strain B13, a genomic island with various catabolic properties., J. Bacteriol., 188, 1999, 10.1128/JB.188.5.1999-2013.2006

Gerischer, 2002, Specific and global regulation of genes associated with the degradation of aromatic compounds in bacteria., J. Mol. Microbiol. Biotechnol., 4, 111

Hacker, 2001, Ecological fitness, genomic islands and bacterial pathogenicity., EMBO Rep., 2, 376, 10.1093/embo-reports/kve097

Harayama, 1994, Codon usage patterns suggest independent evolution of two catabolic operons on toluene-degradative plasmid TOL pWW0 of Pseudomonas putida., J. Mol. Evol., 38, 328, 10.1007/BF00163150

Hildebrand, 2010, Evidence of selection upon genomic GC-content in bacteria., PLoS Genet., 6, 10.1371/journal.pgen.1001107

Hirose, 2021, A new ICEclc subfamily integrative and conjugative element responsible for horizontal transfer of biphenyl and salicylic acid catabolic pathway in the PCB-degrading strain Pseudomonas stutzeri KF716., Microorganisms, 9, 10.3390/microorganisms9122462

Janssen, 2010, The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments., PLoS One, 5, 10.1371/journal.pone.0010433

Jiménez, 2004, Genomic insights in the metabolism of aromatic compounds in Pseudomonas, Pseudomonas, 425, 10.1007/978-1-4419-9088-4_15

Johnson, 2015, Integrative and conjugative elements (ICEs): what they do and how they work., Ann. Rev. Genet., 49, 577, 10.1146/annurev-genet-112414-055018

Juhas, 2009, Genomic islands: tools of bacterial horizontal gene transfer and evolution., FEMS Microbiol. Rev., 33, 376, 10.1111/j.1574-6976.2008.00136.x

Jurka, 2007, Repetitive sequences in complex genomes: structure and evolution., Annu. Rev. Genomics Hum. Genet., 8, 241, 10.1146/annurev.genom.8.080706.092416

Klockgether, 2007, Diversity of the abundant pKLC102/PAGI-2 family of genomic islands in Pseudomonas aeruginosa., J. Bacteriol., 189, 2443, 10.1128/JB.0168806

Kumar, 2016, MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets., Mol. Biol. Evol., 33, 1870, 10.1093/molbev/msw054

Lawley, 2004, Bacterial conjugation in gram-negative bacteria., Plasmid Biol., 13, 203

Lechner, 2009, Genomic island excisions in Bordetella petrii., BMC Microbiol., 9, 10.1186/1471-2180-9-141

Lesic, 2004, Excision of the high-pathogenicity island of Yersinia pseudotuberculosis requires the combined actions of its cognate integrase and Hef, a new recombination directionality factor., Mol. Microbiol., 52, 1337, 10.1111/j.1365-2958.2004.04073.x

Liu, 2019, ICEberg 2.0: an updated database of bacterial integrative and conjugative elements., Nucleic Acids Res., 47, D660, 10.1093/nar/gky1123

Mahajan, 1994, Evidence for the involvement of multiple pathways in the biodegradation of 1-and 2-methylnaphthalene by Pseudomonas putida CSV86., Arch. Microbiol., 161, 425, 10.1007/BF00288954

Miyazaki, 2015, Comparative genome analysis of Pseudomonas knackmussii B13, the first bacterium known to degrade chloroaromatic compounds., Environ. Microbiol., 17, 91, 10.1111/1462-2920.12498

Miyazaki, 2012, Cellular variability of RpoS expression underlies subpopulation activation of an integrative and conjugative element., PLoS Genet., 8, 10.1371/journal.pgen.1002818

Mohan, 2017, Carbon source-dependent inducible metabolism of veratryl alcohol and ferulic acid in Pseudomonas putida CSV86., Appl. Environ. Microbiol., 83, 10.1128/AEM.03326-16

Mohapatra, 2022, Functional genome mining and taxono-genomics reveal eco-physiological traits and species distinctiveness of aromatic-degrading Pseudomonas bharatica sp. nov., Environ. Microbiol. Rep., 14, 464, 10.1111/1758-2229.13066

Mohapatra, 2021, Microbial degradation of naphthalene and substituted naphthalenes: metabolic diversity and genomic insight for bioremediation., Front. Bioeng. Biotechnol., 9, 10.3389/fbioe.2021.602445

Neilson, 1999, Factors influencing expression of luxCDABE and nah genes in Pseudomonas putida RB1353 (NAH7, pUTK9) in dynamic systems., Appl. Environ. Microbiol., 65, 3473, 10.1128/AEM.65.8.3473-3482.1999

Nojiri, 2009, Catabolic plasmids involved in the degradation of polycyclic aromatic hydrocarbons and heteroaromatic compounds, Microbial Megaplasmids, 55, 10.1007/978-3-540-85467-8_3

Obi, 2018, The integrative conjugative element clc (ICEclc) of Pseudomonas aeruginosa JB2., Front. Microbiol., 9, 10.3389/fmicb.2018.01532

Paliwal, 2014, Pseudomonas putida CSV86: a candidate genome for genetic bioaugmentation., PLoS One, 9, 10.1371/journal.pone.0084000

Phale, 2020, Degradation strategies and associated regulatory mechanisms/features for aromatic compound metabolism in bacteria., Adv. Appl. Microbiol., 112, 1, 10.1016/bs.aambs.2020.02.002

Phale, 2021, Eco-physiological portrait of a novel Pseudomonas sp. CSV86: an ideal host/candidate for metabolic engineering and bioremediation., Environ. Microbiol., 1, 10.1111/1462-2920.15694

Phale, 2019, Variability in assembly of degradation operons for naphthalene and its derivative, carbaryl, suggests mobilization through horizontal gene transfer., Genes, 10, 10.3390/genes10080569

Poulin-Laprade, 2015, The extended regulatory networks of SXT/R391 integrative and conjugative elements and IncA/C conjugative plasmids., Front. Microbiol., 6, 10.3389/fmicb.2015.00837

Qian, 2005, Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris., Genome Res., 15, 757, 10.1101/gr.3378705

Rajanna, 2003, The Vibrio pathogenicity island of epidemic Vibrio cholerae forms precise extrachromosomal circular excision products., J. Bacteriol., 185, 6893, 10.1128/JB.185.23.6893-6901.2003

Ravatn, , Low-frequency horizontal transfer of an element containing the chlorocatechol degradation genes from Pseudomonas sp. strain B13 to Pseudomonas putida F1 and to indigenous bacteria in laboratory-scale activated-sludge microcosms., Appl. Environ. Microbiol., 64, 2126, 10.1128/AEM.64.6.2126-2132.1998

Ravatn, , Chromosomal integration, tandem amplification, and deamplification in Pseudomonas putida F1 of a 105-kilobase genetic element containing the chlorocatechol degradative genes from Pseudomonas sp. strain B13., J. Bacteriol., 180, 4360, 10.1128/JB.180.17.4360-4369.1998

Reva, 2005, Differentiation of regions with atypical oligonucleotide composition in bacterial genomes., BMC Bioinformatics, 6, 10.1186/1471-2105-6-251

Rodríguez-Beltrán, 2020, Genetic dominance governs the evolution and spread of mobile genetic elements in bacteria., Proc. Natl. Acad. Sci. U.S.A., 117, 15755, 10.1073/pnas.2001240117

Ryan, 2009, Novel Tn4371-ICE like element in Ralstonia pickettii and genome mining for comparative elements., BMC Microbiol, 9, 10.1186/1471-2180-9-242

Sentchilo, 2009, Intracellular excision and reintegration dynamics of the ICEclc genomic island of Pseudomonas knackmussii sp. strain B13., Mol. Microbiol., 72, 1293, 10.1111/j.1365-2958.2009.06726.x

Singh, 2013, Metabolic regulation and chromosomal localization of carbaryl degradation pathway in Pseudomonas sp. strains C4, C5 and C6., Arch. Microbiol., 195, 521, 10.1007/s00203-013-0903-9

Strnad, 2011, Complete genome sequence of the haloaromatic acid-degrading bacterium Achromobacter xylosoxidans A8., J. Bacteriol., 193, 791, 10.1128/JB.01299-10

van der Meer, 2003, Genomic islands and the evolution of catabolic pathways in bacteria., Curr. Opin. Biotechnol., 14, 248, 10.1016/S0958-1669(03)00058-2

Verma, 2014, Comparative genomic analysis of nine Sphingobium strains: insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways., BMC Genomics, 15, 10.1186/1471-2164-15-1014

Verma, 2019, Catalytic promiscuity of aromatic ring-hydroxylating dioxygenases and their role in the plasticity of xenobiotic compound degradation, Microbial Metabolism of Xenobiotic Compounds, 123, 10.1007/978-981-13-7462-3_6

Wiegand, 2008, Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances., Nat. Protoc., 3, 163, 10.1038/nprot.2007.521

Wozniak, 2009, Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs., PLoS Genet., 5, 10.1371/journal.pgen.1000786

Wozniak, 2010, Integrative and conjugative elements: mosaic mobile genetic elements enabling dynamic lateral gene flow., Nat. Rev. Microbiol., 8, 552, 10.1038/nrmicro2382

Xu, 2019, OrthoVenn2: a web server for whole-genome comparison and annotation of orthologous clusters across multiple species., Nucleic Acids Res., 47, W52, 10.1093/nar/gkz333

Zamarro, 2016, The ICEXTD of Azoarcus sp. CIB, an integrative and conjugative element with aerobic and anaerobic catabolic properties., Environ. Microbiol., 18, 5018, 10.1111/1462-2920.13465

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Frontiers in Microbiology

Tập 13

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