Abstract
Here, we analysed the genomic evolution in extremophilic bacteria using long simple sequence repeats (SSRs). Frequencies of occurrence, relative abundance (RA) and relative density (RD) of long SSRs were analysed in the genomes of extremophilic bacteria. Thermus aquaticus had the most RA and RD of long SSRs in its coding sequences (110.6 and 1408.3), followed by Rhodoferax antarcticus (77.0 and 1187.4). A positive correlation was observed between G + C content and the RA–RD of long SSRs. Geobacillus kaustophilus, Geobacillus thermoleovorans, Halothermothrix orenii, R. antarcticus, and T. aquaticus preferred trinucleotide repeats within their genomes, whereas others preferred a higher number of tetranucleotide repeats. Gene enrichment showed the presence of these long SSRs in metabolic enzyme encoding genes related to stress tolerance. To analyse the functional implications of SSR insertions, three-dimensional protein structure modelling of SSR containing diguanylate cyclase (DGC) gene encoding protein was carried out. Removal of SSR sequence led to an inappropriate folding and instability of the modelled protein structure.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aravind L, Ponting CP (1999) The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol Lett 176:111–116. https://doi.org/10.1111/j.1574-6968.1999.tb13650.x
Breezee J, Cady N, Staley JT (2004) Subfreezing growth of the sea ice bacterium “Psychromonas ingrahamii”. Microb Ecol 47:300–304. https://doi.org/10.1007/s00248-003-1040-9
Brininger C, Spradlin S, Cobani L, Evilia C (2018) The more adaptive to change, the more likely you are to survive: protein adaptation in extremophiles. Semin Cell Dev Biol 84:158–169. https://doi.org/10.1016/j.semcdb.2017.12.016
Cao Y, Fanning S, Proos S, Jordan K, Srikumar S (2017) A review on the applications of next generation sequencing technologies as applied to food-related microbiome studies. Front Microbiol. https://doi.org/10.3389/fmicb.2017.01829
Chattopadhyay MK (2006) Mechanism of bacterial adaptation to low temperature. J Biosci 31:157–165. https://doi.org/10.1007/bf02705244
Cordova LT, Cipolla RM, Swarup A, Long CP, Antoniewicz MR (2017) 13C metabolic flux analysis of three divergent extremely thermophilic bacteria: Geobacillus sp. LC300, Thermus thermophilus HB8, and Rhodothermus marinus DSM 4252. Metab Eng 44:182–190. https://doi.org/10.1016/j.ymben.2017.10.007
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
Ellegren H (2004) Microsatellites: simple sequences with complex evolution. Nat Rev Genet 5:435–445. https://doi.org/10.1038/nrg1348
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 10:62–71
Haney P, Konisky J, Koretke KK, Luthey-Schulten Z, Wolynes PG (1997) Structural basis for thermostability and identification of potential active site residues for adenylate kinases from the archaeal genus Methanococcus. Proteins Struct Funct Bioinform 28:117–130. https://doi.org/10.1002/(sici)1097-0134(199705)28:1%3c117::aid-prot12%3e3.0.co;2-m
Hickey DA, Singer GAC (2004) Genomic and proteomic adaptations to growth at high temperature. Genome Biol 5:117. https://doi.org/10.1186/gb-2004-5-10-117
Hoch JA, Silhavy TJ, Bourret RB (1995) Two-component signal transduction. ASM Press, Washington, DC
Jerome JP, Bell JA, Plovanich-Jones AE, Barrick JE, Brown CT, Mansfield LS (2011) Standing genetic variation in contingency loci drives the rapid adaptation of Campylobacter jejuni to a novel host. PLoS ONE 6:e16399. https://doi.org/10.1371/journal.pone.0016399
Kita K, Ishida A, Tanaka K, Ishikawa S, Yoshida K-i (2020) Complete genome sequence of Thermophilic Bacterium <span class="named-content genus-species" id="named-content-1">Aeribacillus pallidus</span> PI8. Microbiol Resour Announce 9:e00224-e1220. https://doi.org/10.1128/mra.00224-20
Konings WN, Albers SV, Koning S, Driessen AJ (2002) The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments. Ant Van Leeu 81:61–72. https://doi.org/10.1023/a:1020573408652
Liang X, Zhang L, Natarajan SK, Becker DF (2013) Proline mechanisms of stress survival. Antioxid Redox Signal 19:998–1011. https://doi.org/10.1089/ars.2012.5074
Mahfooz S, Srivastava A, Yadav MC, Tahoor A (2019) Comparative genomics in phytopathogenic prokaryotes reveals the higher relative abundance and density of long-SSRs in the smallest prokaryotic genome. 3 Biotech 9:340. https://doi.org/10.1007/s13205-019-1872-8
Mahfooz S, Singh P, Akhter Y (2022) A comparative study of microsatellites among crocodiles and development of genomic resources for the critically endangered Indian gharial. Genetica 150:67–75. https://doi.org/10.1007/s10709-021-00148-0
Matsushita K, Azuma Y, Kosaka T, Yakushi T, Hoshida H, Akada R, Yamada M (2016) Genomic analyses of thermotolerant microorganisms used for high-temperature fermentations. Biosci Biotechnol Biochem 80:655–668. https://doi.org/10.1080/09168451.2015.1104235
Matsutani M, Hirakawa H, Nishikura M, Soemphol W, Ali IA, Yakushi T, Matsushita K (2011) Increased number of Arginine-based salt bridges contributes to the thermotolerance of thermotolerant acetic acid bacteria, Acetobacter tropicalis SKU1100. Biochem Biophys Res Commun 409:120–124. https://doi.org/10.1016/j.bbrc.2011.04.126
McDonald MJ (2019) Microbial experimental evolution—a proving ground for evolutionary theory and a tool for discovery. EMBO Rep 20:e46992–e46992. https://doi.org/10.15252/embr.201846992
Moxon R, Bayliss C, Hood D (2006) Bacterial contingency loci: the role of simple sequence DNA repeats in bacterial adaptation. Annu Rev Genet 40:307–333. 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 USA 104:8472–8477. https://doi.org/10.1073/pnas.0702412104
Muhd Sakaff MKL, Abdul Rahman AY, Saito JA, Hou S, Alam M (2012) Complete genome sequence of the thermophilic bacterium Geobacillus thermoleovorans CCB_US3_UF5. J Bacteriol 194:1239–1239. https://doi.org/10.1128/JB.06580-11
Ortega G, Diercks T, Millet O (2015) Halophilic protein adaptation results from synergistic residue–ion interactions in the folded and unfolded states. Chem Biol 22:1597–1607. https://doi.org/10.1016/j.chembiol.2015.10.010
Panja AS, Bandopadhyay B, Maiti S (2015) Protein thermostability is owing to their preferences to non-polar smaller volume amino acids, variations in residual physico-chemical properties and more salt-bridges. PLoS ONE 10:e0131495. https://doi.org/10.1371/journal.pone.0131495
Panja AS, Maiti S, Bandyopadhyay B (2020) Protein stability governed by its structural plasticity is inferred by physicochemical factors and salt bridges. Sci Rep 10:1822. https://doi.org/10.1038/s41598-020-58825-7
Raymond-Bouchard I, Goordial J, Zolotarov Y, Ronholm J, Stromvik M, Bakermans C, Whyte LG (2018) Conserved genomic and amino acid traits of cold adaptation in subzero-growing Arctic permafrost bacteria. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiy023
Russell RJ, Ferguson JM, Hough DW, Danson MJ, Taylor GL (1997) The crystal structure of citrate synthase from the hyperthermophilic archaeon pyrococcus furiosus at 1.9 A resolution. Biochemistry 36:9983–9994. https://doi.org/10.1021/bi9705321
Ryjenkov DA, Tarutina M, Moskvin OV, Gomelsky M (2005) Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J Bacteriol 187:1792–1798. https://doi.org/10.1128/jb.187.5.1792-1798.2005
Sant’Anna FH, Lebedinsky AV, Sokolova TG, Robb FT, Gonzalez JM (2015) Analysis of three genomes within the thermophilic bacterial species Caldanaerobacter subterraneus with a focus on carbon monoxide dehydrogenase evolution and hydrolase diversity. BMC Genomics 16:757. https://doi.org/10.1186/s12864-015-1955-9
Sharma S, Sharma S, Ahmed M, Akhter Y, Chatterjee S (2021) Ornithine carbamoyltransferase from psychrophiles to thermophiles: structural evolution of catalytic fold to accommodate physiological diversity. Extremophiles 25:15–24. https://doi.org/10.1007/s00792-020-01208-7
Tahoor A, Khan JA, Mahfooz S (2019) A comparative survey of microsatellites among wild and domestic cat provides valuable resources for marker development. Mol Biol Rep 46:3025–3033. https://doi.org/10.1007/s11033-019-04739-1
Tian X, Strassmann JE, Queller DC (2011) Genome nucleotide composition shapes variation in simple sequence repeats. Mol Biol Evol 28:899–909. https://doi.org/10.1093/molbev/msq266
Treangen TJ, Messeguer X (2006) M-GCAT: interactively and efficiently constructing large-scale multiple genome comparison frameworks in closely related species. BMC Bioinform 7:433. https://doi.org/10.1186/1471-2105-7-433
Wadapurkar RM, Vyas R (2018) Computational analysis of next generation sequencing data and its applications in clinical oncology. Inf Med Unlocked 11:75–82. https://doi.org/10.1016/j.imu.2018.05.003
Acknowledgements
We thank the Department of Biotechnology, Babasaheb Bhimrao Ambedkar University for providing us the required infrastructure for the presented work.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None.
Additional information
Communicated by L. Huang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Mahfooz, S., Shankar, G., Narayan, J. et al. Simple sequence repeat insertion induced stability and potential ‘gain of function’ in the proteins of extremophilic bacteria. Extremophiles 26, 17 (2022). https://doi.org/10.1007/s00792-022-01265-0
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00792-022-01265-0