Abstract
Pathogenic bacteria use phase variation of surface molecules and other characteristics as a significant adaptation mechanism. Repetitive sequences made up of numerous identical repeat units can be found in many phase variable genes. Here, we investigated the frequency and distribution of long-SSRs (Simple Sequence Repeats) in 15 human pathogenic Staphylococcus, Streptococcus, and Enterococcus bacteria. Long-SSRs were found to be distributed differently in the genic and inter-genic sequences. In the genic sequences, 61.3 SSRs were discovered on average, while 16.2 SSRs were found in the intergenic regions. Staphylococcus exhibited the highest frequency of SSRs, followed by Enterococcus, and Streptococcus had the lowest frequency of SSRs. Higher A + T content was found to be the best predictor of long-SSR in these human pathogens. Tetranucleotide repeats predominated in inte-rgenic regions, while trinucleotide repeats were in the majority in genic regions. In human pathogenic Streptococcus and Staphylococcus bacteria, genus-specific encoding of amino acids by tri-nucleotide SSRs was observed. Based on the presence of SSRs in housekeeping genes, a genetic relationship between these human pathogenic bacteria was constructed and compared to a phylogeny based on the 16 S ribosomal RNA gene.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- SSR:
-
Simple sequence repeats.
- RA:
-
Relative abundance.
- RD:
-
Relative density.
- PIC:
-
Polymorphism information content.
- PANNZER:
-
Protein ANNotation with Z-scoRE.
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes.
- GO:
-
Gene ontology.
References
Andrewes FW, Horder TJ (1906) A study of the streptococci pathogenic for man. The Lancet 168(4333):708–713. https://doi.org/10.1016/S0140-6736(01)31538-6
Bayliss CD (2009) Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol Rev 33(3):504–520. https://doi.org/10.1111/j.1574-6976.2009.00162.x
Becker K, Heilmann C, Peters G (2014) Coagulase-negative staphylococci. Clin Microbiol Rev 27(4):870–926. https://doi.org/10.1128/CMR.00109-13
Botstein D, White RL, Skolnick M, Davis RW (1980) Construction of a genetic linkage map in man using restriction fragment length polymorphisms. Am J Hum Genet 32(3):314–331
Champney WS, Chittum HS, Tober CL (2003) A 50S ribosomal subunit precursor particle is a substrate for the ErmC methyltransferase in Staphylococcus aureus cells. Curr Microbiol 46(6):453–460. https://doi.org/10.1007/s00284-002-3901-8
da Maia LC, Palmieri DA, de Souza VQ, Kopp MM, de Carvalho FIF, Costa de Oliveira A (2008) SSR Locator: Tool for Simple Sequence Repeat Discovery Integrated with Primer Design and PCR Simulation. Int J Plant Genomics 2008:412696. https://doi.org/10.1155/2008/412696
Datta S, Mahfooz S, Singh P, Choudhary AK, Singh F, Kumar S (2010) Cross-genera amplification of informative microsatellite markers from common bean and lentil for the assessment of genetic diversity in pigeonpea. Physiol Mol Biol Plants 16(2):123–134. https://doi.org/10.1007/s12298-010-0014-x
De Bolle X, Bayliss CD, Field D, van de Ven T, Saunders NJ, Hood DW, Moxon ER (2000) The length of a tetranucleotide repeat tract in Haemophilus influenzae determines the phase variation rate of a gene with homology to type III DNA methyltransferases. Mol Microbiol 35(1):211–222. https://doi.org/10.1046/j.1365-2958.2000.01701.x
Feehily C, Karatzas KA (2013) Role of glutamate metabolism in bacterial responses towards acid and other stresses. J Appl Microbiol 114(1):11–24. https://doi.org/10.1111/j.1365-2672.2012.05434.x
Field D, Wills C (1998) Abundant microsatellite polymorphism in Saccharomyces cerevisiae, and the different distributions of microsatellites in eight prokaryotes and S. cerevisiae, result from strong mutation pressures and a variety of selective forces. Proc Natl Acad Sci U.S.A 95 (4):1647–1652
Fitzgerald JR, Musser JM (2001) Evolutionary genomics of pathogenic bacteria. Trends Microbiol 9(11):547–553. https://doi:10.1016/s0966-842x(01)02228-4
Geng H, Hao L, Cheng Y, Wang C, Huang S, Wei W, Yang R, Li H, Liu S, Yu H, Lu H (2020) Interaction between CA repeat microsatellites and HIF1α regulated the transcriptional activity of porcine IGF1 promoter. J Appl Genet 61(1):105–112. doi:https://doi.org/10.1007/s13353-019-00529-4
Gillner DM, Becker DP, Holz RC (2013) Lysine biosynthesis in bacteria: a metallodesuccinylase as a potential antimicrobial target. J Biol Inorg Chem 18(2):155–163. https://doi.org/10.1007/s00775-012-0965-1
Gur-Arie R, Cohen CJ, Eitan Y, Shelef L, Hallerman EM, Kashi Y (2000) Simple sequence repeats in Escherichia coli: abundance, distribution, composition, and polymorphism. Genome Res 10(1):62–71. https://doi.org/10.1101/gr.10.1.62
Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9(10):486–493. https://doi.org/10.1016/s0966-842x(01)02175-8
Hwang SR, Garza CZ, Wegrzyn JL, Hook VY (2005) Demonstration of GTG as an alternative initiation codon for the serpin endopin 2B-2. Biochem Biophys Res Commun 327(3):837–844. https://doi.org/10.1016/j.bbrc.2004.12.053
Kaiser Julienne C, Heinrichs David E, Garsin D (2018) A Branching Out: Alterations in Bacterial Physiology and Virulence Due to Branched-Chain Amino Acid Deprivation. mBio 9(5):e01188–e01118. https://doi.org/10.1128/mBio.01188-18
Kosecka-Strojek M, Sabat AJ, Akkerboom V, Kooistra-Smid AMD, Miedzobrodzki J, Friedrich AW (2019) Development of a reference data set for assigning Streptococcus and Enterococcus species based on next generation sequencing of the 16S–23S rRNA region. Antimicrob Resist In 8(1):178. https://doi.org/10.1186/s13756-019-0622-3
Krinos CM, Coyne MJ, Weinacht KG, Tzianabos AO, Kasper DL, Comstock LE (2001) Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414(6863):555–558. https://doi.org/10.1038/35107092
Krismer B, Weidenmaier C, Zipperer A, Peschel A (2017) The commensal lifestyle of Staphylococcus aureus and its interactions with the nasal microbiota. Nat Rev Microbiol 15(11):675–687. https://doi.org/10.1038/nrmicro.2017.104
Lawson MJ, Zhang L (2008) Housekeeping and tissue-specific genes differ in simple sequence repeats in the 5’-UTR region. Gene 407(1–2):54–62. doi:https://doi.org/10.1016/j.gene.2007.09.017
Lin WH, Kussell E (2012) Evolutionary pressures on simple sequence repeats in prokaryotic coding regions. Nucleic acids Res 40(6):2399–2413. https://doi.org/10.1093/nar/gkr1078
Loewe L, Hill WG (2010) The population genetics of mutations: good, bad and indifferent. Philos Trans R Soc Lond B Biol Sci 365(1544):1153–1167. doi:https://doi.org/10.1098/rstb.2009.0317
Mahfooz S, Shankar G, Narayan J, Singh P, Akhter Y (2022) Simple sequence repeat insertion induced stability and potential ‘gain of function’ in the proteins of extremophilic bacteria. Extremophiles 26(2):17. https://doi.org/10.1007/s00792-022-01265-0
Mahfooz S, Singh SP, Mishra N, Mishra A (2017) A Comparison of Microsatellites in Phytopathogenic Aspergillus Species in Order to Develop Markers for the Assessment of Genetic Diversity among Its Isolates. Front Microbiol 8:1774. https://doi.org/10.3389/fmicb.2017.01774
Mahfooz S, Singh SP, Rakh R, Bhattacharya A, Mishra N, Singh PC, Chauhan PS, Nautiyal CS, Mishra A (2016) A Comprehensive Characterization of Simple Sequence Repeats in the Sequenced Trichoderma Genomes Provides Valuable Resources for Marker Development. Front Microbiol 7:575. https://doi.org/10.3389/fmicb.2016.00575
Mahfooz S, Srivastava A, Srivastava AK, Arora DK (2015) A comparative analysis of distribution and conservation of microsatellites in the transcripts of sequenced Fusarium species and development of genic-SSR markers for polymorphism analysis. FEMS Microbiol Let 362(17). https://doi.org/10.1093/femsle/fnv131
Martin P, Makepeace K, Hill SA, Hood DW, Moxon ER (2005) Microsatellite instability regulates transcription factor binding and gene expression. Proc Natl Acad Sci U S A 102(10):3800–3804. https://doi.org/10.1073/pnas.0406805102
Metzgar D, Bytof J, Wills C (2000) Selection against frameshift mutations limits microsatellite expansion in coding DNA. Genome Res 10(1):72–80
Moxon R, Bayliss C, Hood D (2006) Bacterial Contingency Loci: The Role of Simple Sequence DNA Repeats in Bacterial Adaptation. Annu Rev Genet 40(1):307–333. https://doi.org/10.1146/annurev.genet.40.110405.090442
Mrazek J, Guo X, Shah A (2007) Simple sequence repeats in prokaryotic genomes. Proc Natl Acad Sci U S A 104(20):8472–8477. https://doi.org/10.1073/pnas.0702412104
Perna NT, Plunkett G 3, Burland V, Mau B, Glasner JD, Rose DJ, Mayhew GF, Evans PS, Gregor J, Kirkpatrick HA, Pósfai G, Hackett J, Klink S, Boutin A, Shao Y, Miller L, Grotbeck EJ, Davis NW, Lim A, Dimalanta ET, Potamousis KD, Apodaca J, Anantharaman TS, Lin J, Yen G, Schwartz DC, Welch RA, Blattner FR (2001) Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature 409(6819):529–533. https://doi.org/10.1038/35054089
R Core Development Core Team (2021) : R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rohlf FJ (1998) On applications of geometric morphometrics to studies of ontogeny and phylogeny. Syst Biol 47(1):147–158 discussion 159–167
Rossi CC, Pereira MF, Giambiagi-deMarval M (2020) Underrated Staphylococcus species and their role in antimicrobial resistance spreading. Genet Mol Biol 43(1 suppl 2):e20190065. https://doi.org/10.1590/1678-4685-gmb-2019-0065
Safdar A, Armstrong D (2019) Staphylococcus, Streptococcus, and Enterococcus. In: Safdar A (ed) Principles and Practice of Transplant Infectious Diseases. Springer New York, New York, NY, pp 419–445. https://doi:10.1007/978-1-4939-9034-4_24
Schleifer KH, Kilpper-Bälz R (1984) Transfer of Streptococcus faecalis and Streptococcus faecium to the Genus Enterococcus nom. rev. as Enterococcus faecalis comb. nov. and Enterococcus faecium comb. nov. Int J Syst Evol Micr 34(1):31–34. https://doi.org/10.1099/00207713-34-1-31
Song X, Yang T, Zhang X, Yuan Y, Yan X, Wei Y, Zhang J, Zhou C (2021) Comparison of the Microsatellite Distribution Patterns in the Genomes of Euarchontoglires at the Taxonomic Level. Front Genet 12(227). https://doi.org/10.3389/fgene.2021.622724
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739. https://doi.org/10.1093/molbev/msr121
Woolhouse ME, Taylor LH, Haydon DT (2001) Population biology of multihost pathogens. Science 292(5519):1109–1112. https://doi.org/10.1126/science.1059026
Acknowledgements
This research has been funded by Scientific Research Deanship at the University of Ha’il – Saudi Arabia through project number RG-21 152.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
None declared.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mahfooz, S., Narayan, J., Ahmed, R.M.E. et al. Comparative genomics reveals genus specific encoding of amino acids by tri-nucleotide SSRs in human pathogenic Streptococcus and Staphylococcus bacteria. Biologia 77, 2955–2966 (2022). https://doi.org/10.1007/s11756-022-01143-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-022-01143-2