Bacterial chromosomal mobility via lateral transduction exceeds that of classical mobile genetic elements

被引:53
作者
Humphrey, Suzanne [1 ]
Fillol-Salom, Alfred [1 ,2 ]
Quiles-Puchalt, Nuria [1 ,2 ]
Ibarra-Chavez, Rodrigo [1 ,3 ]
Haag, Andreas F. [1 ]
Chen, John [4 ]
Penades, Jose R. [1 ,2 ,5 ]
机构
[1] Univ Glasgow, Inst Infect Immun & Inflammat, Glasgow G12 8TA, Lanark, Scotland
[2] Imperial Coll London, MRC Ctr Mol Bacteriol & Infect, London SW7 2AZ, England
[3] Univ Copenhagen, Dept Biol, Sect Microbiol, Univ Pk 15,Bldg 1, DK-2100 Copenhagen, Denmark
[4] Natl Univ Singapore, Yong Loo Lin Sch Med, Dept Microbiol & Immunol, 5 Sci Dr 2, Singapore, Singapore
[5] Univ CEU Cardenal Herrera, Fac Ciencias Salud, Dept Ciencias Biomed, Valencia 46113, Spain
基金
英国医学研究理事会; 英国生物技术与生命科学研究理事会; 英国惠康基金;
关键词
STAPHYLOCOCCUS-AUREUS; PATHOGENICITY ISLAND; ESCHERICHIA-COLI; CONJUGATIVE ELEMENTS; VIRULENCE PLASMID; SALMONELLA; PHAGE; RESISTANCE; RECOMBINATION; EVOLUTION;
D O I
10.1038/s41467-021-26004-5
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
It is commonly assumed that the horizontal transfer of most bacterial chromosomal genes is limited, in contrast to the frequent transfer observed for typical mobile genetic elements. However, this view has been recently challenged by the discovery of lateral transduction in Staphylococcus aureus, where temperate phages can drive the transfer of large chromosomal regions at extremely high frequencies. Here, we analyse previously published as well as new datasets to compare horizontal gene transfer rates mediated by different mechanisms in S. aureus and Salmonella enterica. We find that the horizontal transfer of core chromosomal genes via lateral transduction can be more efficient than the transfer of classical mobile genetic elements via conjugation or generalized transduction. These results raise questions about our definition of mobile genetic elements, and the potential roles played by lateral transduction in bacterial evolution. It is commonly thought that horizontal transfer of most bacterial chromosomal genes is limited, in comparison with the frequent transfer of mobile genetic elements. Humphrey et al. show that, actually, phage-mediated lateral transduction of core chromosomal genes can be more efficient than the transfer of mobile genetic elements via conjugation or generalized transduction.
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页数:13
相关论文
共 59 条
[21]   Lateral transduction is inherent to the life cycle of the archetypical Salmonella phage P22 [J].
Fillol-Salom, Alfred ;
Bacigalupe, Rodrigo ;
Humphrey, Suzanne ;
Chiang, Yin Ning ;
Chen, John ;
Penades, Jose R. .
NATURE COMMUNICATIONS, 2021, 12 (01)
[22]   Bacteriophages benefit from generalized transduction [J].
Fillol-Salom, Alfred ;
Alsaadi, Ahlam ;
de Sousa, Jorge A. Moura ;
Zhong, Li ;
Foster, Kevin R. ;
Rocha, Eduardo P. C. ;
Penades, Jose R. ;
Ingmer, Hanne ;
Haaber, Jakob .
PLOS PATHOGENS, 2019, 15 (07)
[23]   Phage-inducible chromosomal islands are ubiquitous within the bacterial universe [J].
Fillol-Salom, Alfred ;
Martinez-Rubio, Roser ;
Abdulrahman, Rezheen F. ;
Chen, John ;
Davies, Robert ;
Penades, Jose R. .
ISME JOURNAL, 2018, 12 (09) :2114-2128
[24]   A regulatory cascade controls Staphylococcus aureus pathogenicity island activation [J].
Haag, Andreas F. ;
Podkowik, Magdalena ;
Ibarra-Chavez, Rodrigo ;
Gallego del Sol, Francisca ;
Ram, Geeta ;
Chen, John ;
Marina, Alberto ;
Novick, Richard P. ;
Penades, Jose R. .
NATURE MICROBIOLOGY, 2021, 6 (10) :1300-+
[25]   Network analyses structure genetic diversity in independent genetic worlds [J].
Halary, Sebastien ;
Leigh, Jessica W. ;
Cheaib, Bachar ;
Lopez, Philippe ;
Bapteste, Eric .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (01) :127-132
[26]   Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages [J].
Hensel, M ;
Shea, JE ;
Waterman, SR ;
Mundy, R ;
Nikolaus, T ;
Banks, G ;
Vazquez-Torres, A ;
Gleeson, C ;
Fang, FC ;
Holden, DW .
MOLECULAR MICROBIOLOGY, 1998, 30 (01) :163-174
[27]   Integrative and Conjugative Elements (ICEs): What They Do and How They Work [J].
Johnson, Christopher M. ;
Grossman, Alan D. .
ANNUAL REVIEW OF GENETICS, VOL 49, 2015, 49 :577-601
[28]   Bacterial transformation: distribution, shared mechanisms and divergent control [J].
Johnston, Calum ;
Martin, Bernard ;
Fichant, Gwennaele ;
Polard, Patrice ;
Claverys, Jean-Pierre .
NATURE REVIEWS MICROBIOLOGY, 2014, 12 (03) :181-196
[29]   TRANSFER OF THE CONJUGAL TETRACYCLINE RESISTANCE TRANSPOSON TN916 FROM STREPTOCOCCUS-FAECALIS TO STAPHYLOCOCCUS-AUREUS AND IDENTIFICATION OF SOME INSERTION SITES IN THE STAPHYLOCOCCAL CHROMOSOME [J].
JONES, JM ;
YOST, SC ;
PATTEE, PA .
JOURNAL OF BACTERIOLOGY, 1987, 169 (05) :2121-2131
[30]   Contribution of SPI-4 genes to the virulence of Salmonella enterica [J].
Kiss, Tuende ;
Morgan, Eirwen ;
Nagy, Gabor .
FEMS MICROBIOLOGY LETTERS, 2007, 275 (01) :153-159