Genome-wide Comparative Analysis of Clinical and Environmental Strains of the Opportunistic Pathogen ()

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2024 Nov 21

PMID 39568992

Authors

Magdalena Szuplewska

Dorota Sentkowska

Robert Lasek

Przemyslaw Decewicz

Mateusz Halucha

Lukasz Funk

Cora Chmielowska

Dariusz Bartosik

Affiliations

Soon will be listed here.

Abstract

Introduction: is the first species in the genus to be implicated in opportunistic infections in humans. As a result, strains provide a valuable model for exploring how bacteria shift from a saprophytic to a pathogenic lifestyle, as well as for investigating the role of horizontally transferred DNA in this transition. In order to gain deeper insights into the unique characteristics of this bacterium and the molecular mechanisms underlying its opportunistic behavior, a comparative physiological and genomic analysis of strains was performed.

Results: Complete genomic sequences of 7 isolates (both clinical and environmental) were obtained and analyzed. All genomes have a multipartite structure comprising numerous extrachromosomal replicons (59 different ECRs in total), including large chromids of the DnaA-like and RepB families. Within the mobile part of the genomes (ECRs and transposable elements, TEs), a novel non-autonomous MITE-type element was identified. Detailed genus-wide comparative genomic analysis permitted the identification of -specific genes, including several putative virulence determinants. One of these, the URE gene cluster, determines the ureolytic activity of strains-a unique feature among spp. This activity is induced by the inclusion of urea in the growth medium and is dependent on the presence of an intact regulatory gene, which presumably regulates expression of nickel (urease cofactor) transporter genes.

Discussion: This in-depth comparative analysis provides a detailed insight into the structure, composition and properties of genomes. Several predicted virulence determinants (including URE gene clusters) were identified within ECRs, indicating an important role for the flexible genome in determining the opportunistic properties of this bacterium.

References

Czarnecki J, Bartosik D . Diversity of Methylotrophy Pathways in the Genus (). Curr Issues Mol Biol. 2019; 33:117-132. DOI: 10.21775/cimb.033.117. View

Choi J, Cho Y, Lee J, Shin H, Lee I . Bacterial Contamination and Disinfection Status of Laryngoscopes Stored in Emergency Crash Carts. J Prev Med Public Health. 2017; 50(3):158-164. PMC: 5495683. DOI: 10.3961/jpmph.17.013. View

Pukall R, Laroche M, Kroppenstedt R, Schumann P, Stackebrandt E, Ulber R . Paracoccus seriniphilus sp. nov., an L-serine-dehydratase-producing coccus isolated from the marine bryozoan Bugula plumosa. Int J Syst Evol Microbiol. 2003; 53(Pt 2):443-447. DOI: 10.1099/ijs.0.02352-0. View

Makino K, Kim S, Shinagawa H, Amemura M, Nakata A . Molecular analysis of the cryptic and functional phn operons for phosphonate use in Escherichia coli K-12. J Bacteriol. 1991; 173(8):2665-72. PMC: 207835. DOI: 10.1128/jb.173.8.2665-2672.1991. View

Shun Fu M, Coelho C, De Leon-Rodriguez C, Rossi D, Camacho E, Jung E . Cryptococcus neoformans urease affects the outcome of intracellular pathogenesis by modulating phagolysosomal pH. PLoS Pathog. 2018; 14(6):e1007144. PMC: 6021110. DOI: 10.1371/journal.ppat.1007144. View

Lee J, Kim Y, Choi T, Lee W, Kim Y . Paracoccus haeundaensis sp. nov., a Gram-negative, halophilic, astaxanthin-producing bacterium. Int J Syst Evol Microbiol. 2004; 54(Pt 5):1699-1702. DOI: 10.1099/ijs.0.63146-0. View

Schneider D, Faure D, Barriere A, Coursange E, Blot M . A broad-host-range plasmid for isolating mobile genetic elements in gram-negative bacteria. Plasmid. 2000; 44(2):201-7. DOI: 10.1006/plas.2000.1483. View

Siller H, Rainey F, Stackebrandt E, Winter J . Isolation and characterization of a new gram-negative, acetone-degrading, nitrate-reducing bacterium from soil, Paracoccus solventivorans sp. nov. Int J Syst Bacteriol. 1996; 46(4):1125-30. DOI: 10.1099/00207713-46-4-1125. View

Ali M, Li X, Tang Q, Liu X, Chen F, Xiao J . Regulation of Inducible Potassium Transporter KdpFABC by the KdpD/KdpE Two-Component System in . Front Microbiol. 2017; 8:570. PMC: 5401905. DOI: 10.3389/fmicb.2017.00570. View

10.

Funke G, Frodl R, Sommer H . First comprehensively documented case of Paracoccus yeei infection in a human. J Clin Microbiol. 2004; 42(7):3366-8. PMC: 446255. DOI: 10.1128/JCM.42.7.3366-3368.2004. View

11.

Horsman G, Zechel D . Phosphonate Biochemistry. Chem Rev. 2016; 117(8):5704-5783. DOI: 10.1021/acs.chemrev.6b00536. View

12.

Lipszyc A, Szuplewska M, Bartosik D . How Do Transposable Elements Activate Expression of Transcriptionally Silent Antibiotic Resistance Genes?. Int J Mol Sci. 2022; 23(15). PMC: 9330008. DOI: 10.3390/ijms23158063. View

13.

Urakami T, Araki H, Oyanagi H, Suzuki K, Komagata K . Paracoccus aminophilus sp. nov. and Paracoccus aminovorans sp. nov., which utilize N,N-dimethylformamide. Int J Syst Bacteriol. 1990; 40(3):287-91. DOI: 10.1099/00207713-40-3-287. View

14.

Hassouni M, Chambost J, Expert D, Van Gijsegem F, Barras F . The minimal gene set member msrA, encoding peptide methionine sulfoxide reductase, is a virulence determinant of the plant pathogen Erwinia chrysanthemi. Proc Natl Acad Sci U S A. 1999; 96(3):887-92. PMC: 15320. DOI: 10.1073/pnas.96.3.887. View

15.

Pasquale L, Maurano A, Cengia G, Da Massa Carrara P, Germana B, Graziani M . Infection prevention in endoscopy practice: comparative evaluation of re-usable vs single-use endoscopic valves. Infect Prev Pract. 2021; 3(2):100123. PMC: 8336158. DOI: 10.1016/j.infpip.2021.100123. View

16.

Tatusov R, Fedorova N, Jackson J, Jacobs A, Kiryutin B, Koonin E . The COG database: an updated version includes eukaryotes. BMC Bioinformatics. 2003; 4:41. PMC: 222959. DOI: 10.1186/1471-2105-4-41. View

17.

Chistoserdova L . Modularity of methylotrophy, revisited. Environ Microbiol. 2011; 13(10):2603-22. DOI: 10.1111/j.1462-2920.2011.02464.x. View

18.

Dziewit L, Baj J, Szuplewska M, Maj A, Tabin M, Czyzkowska A . Insights into the transposable mobilome of Paracoccus spp. (Alphaproteobacteria). PLoS One. 2012; 7(2):e32277. PMC: 3281130. DOI: 10.1371/journal.pone.0032277. View

19.

Aliste-Fernandez M, Sanfeliu-Sala I, Sanchez-Delgado J . Bacteremia caused by Paracoccus yeei in patient with compensated cirrhosis of the liver. Enferm Infecc Microbiol Clin (Engl Ed). 2020; 38(9):451-452. DOI: 10.1016/j.eimc.2020.01.013. View

20.

Liu X, Wang B, Jiang C, Liu S . Paracoccus sulfuroxidans sp. nov., a sulfur oxidizer from activated sludge. Int J Syst Evol Microbiol. 2006; 56(Pt 11):2693-2695. DOI: 10.1099/ijs.0.64548-0. View