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Novel Mobile Integrons and Strain-Specific Integrase Genes within Shewanella spp. Unveil Multiple Lateral Genetic Transfer Events within The Genus.

ABSTRACT: Shewanella spp. are Gram-negative bacteria that thrive in aquatic niches and also can cause infectious diseases as opportunistic pathogens. Chromosomal (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems and their genetic surroundings in the genus. We identified 22 integrase gene types, 17 of which were newly described, showing traits of multiple events of lateral genetic transfer (LGT). Phylogenetic analysis showed that most of them were strain-specific, except for Shewanella algae, where SonIntIA-like may have co-evolved within the host as typical CIs. It is noteworthy that co-existence of up to five different integrase genes within a strain, as well as their wide dissemination to Alteromonadales, Vibrionales, Chromatiales, Oceanospirillales and Enterobacterales was observed. In addition, identification of two novel MIs suggests that continuous LGT events may have occurred resembling the behavior of class 1 integrons. The constant emergence of determinants associated to antimicrobial resistance worldwide, concomitantly with novel MIs in strains capable to harbor several types of integrons, may be an alarming threat for the recruitment of novel antimicrobial resistance gene cassettes in the genus Shewanella, with its consequent contribution towards multidrug resistance in clinical isolates.

SUBMITTER: Ayala Nunez T

PROVIDER: S-EPMC9229058 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Novel Mobile Integrons and Strain-Specific Integrase Genes within Shewanella spp. Unveil Multiple Lateral Genetic Transfer Events within The Genus.

Ayala Nuñez Teolincacihuatl T Cerbino Gabriela N GN Rapisardi María Florencia MF Quiroga Cecilia C Centrón Daniela D

Microorganisms 20220526 6

Shewanella spp. are Gram-negative bacteria that thrive in aquatic niches and also can cause infectious diseases as opportunistic pathogens. Chromosomal (CI) and mobile integrons (MI) were previously described in some Shewanella isolates. Here, we evaluated the occurrence of integrase genes, the integron systems and their genetic surroundings in the genus. We identified 22 integrase gene types, 17 of which were newly described, showing traits of multiple events of lateral genetic tr ...[more]

PMID: 35744620

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Project description:A novel bacterial behavior called congregation was recently described in Shewanella oneidensis MR-1 as the accumulation of cells around insoluble electron acceptors (IEA). It is the result of a series of "run-and-reversal" events enabled by modulation of swimming speed and direction. The model proposed that the swimming cells constantly sense their surroundings with specialized outer membrane cytochromes capable of extracellular electron transport (EET). Up to this point, neither the congregation nor attachment behavior have been studied in any other strains. In this study, the wild type of S. oneidensis MR-1 and several deletion mutants as well as eight other Shewanella strains (Shewanella putrefaciens CN32, S. sp. ANA-3, S. sp. W3-18-1, Shewanella amazonensis SB2B, Shewanella loihica PV-4, Shewanella denitrificans OS217, Shewanella baltica OS155, and Shewanella frigidimarina NCIMB400) were screened for the ability to congregate. To monitor congregation and attachment, specialized cell-tracking techniques, as well as a novel cell accumulation after photo-bleaching (CAAP) confocal microscopy technique were utilized in this study. We found a strong correlation between the ability of strain MR-1 to accumulate on mineral surface and the presence of key EET genes such as mtrBC/omcA (SO_1778, SO_1776, and SO_1779) and gene coding for methyl-accepting protein (MCPs) with Ca+ channel chemotaxis receptor (Cache) domain (SO_2240). These EET and taxis genes were previously identified as essential for characteristic run and reversal swimming around IEA surfaces. CN32, ANA-3, and PV-4 congregated around both Fe(OH)3 and MnO2. Two other Shewanella spp. showed preferences for one oxide over the other: preferences that correlated with the metal content of the environments from which the strains were isolated: e.g., W3-18-1, which was isolated from an iron-rich habitat congregated and attached preferentially to Fe(OH)3, while SB2B, which was isolated from a MnO2-rich environment, preferred MnO2.

Project description:BackgroundIntegrons are found in hundreds of environmental bacterial species, but are mainly known as the agents responsible for the capture and spread of antibiotic-resistance determinants between Gram-negative pathogens. The SOS response is a regulatory network under control of the repressor protein LexA targeted at addressing DNA damage, thus promoting genetic variation in times of stress. We recently reported a direct link between the SOS response and the expression of integron integrases in Vibrio cholerae and a plasmid-borne class 1 mobile integron. SOS regulation enhances cassette swapping and capture in stressful conditions, while freezing the integron in steady environments. We conducted a systematic study of available integron integrase promoter sequences to analyze the extent of this relationship across the Bacteria domain.ResultsOur results showed that LexA controls the expression of a large fraction of integron integrases by binding to Escherichia coli-like LexA binding sites. In addition, the results provide experimental validation of LexA control of the integrase gene for another Vibrio chromosomal integron and for a multiresistance plasmid harboring two integrons. There was a significant correlation between lack of LexA control and predicted inactivation of integrase genes, even though experimental evidence also indicates that LexA regulation may be lost to enhance expression of integron cassettes.ConclusionsAncestral-state reconstruction on an integron integrase phylogeny led us to conclude that the ancestral integron was already regulated by LexA. The data also indicated that SOS regulation has been actively preserved in mobile integrons and large chromosomal integrons, suggesting that unregulated integrase activity is selected against. Nonetheless, additional adaptations have probably arisen to cope with unregulated integrase activity. Identifying them may be fundamental in deciphering the uneven distribution of integrons in the Bacteria domain.

Dataset Information

Novel Mobile Integrons and Strain-Specific Integrase Genes within Shewanella spp. Unveil Multiple Lateral Genetic Transfer Events within The Genus.

Publications

Novel Mobile Integrons and Strain-Specific Integrase Genes within <i>Shewanella</i> spp. Unveil Multiple Lateral Genetic Transfer Events within The Genus.

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