Abstract
Pho regulon is a highly evolved and conserved mechanism across the microbes to fulfil their phosphate need. In this study, 52 proteobacteria genomes were analyzed for the presence of phosphorus acquisition genes, their pattern of arrangement and copy numbers. The diverse genetic architecture of the Pho regulon genes indicates the evolutionary challenge of nutrient limitation, particularly phosphorus, faced by bacteria in their environment. The incongruence between the Pho regulon proteins phylogeny and species phylogeny along with the presence of additional copies of pstS and pstB genes, having cross similarity with other genera, suggest the possibility of horizontal gene transfer event. The substitution rate analysis and multiple sequence alignment of the Pho regulon proteins were analyzed to gain additional insight into the evolution of the Pho regulon system. This comprehensive study confirms that genes perform the regulatory function (phoBR) were vertically inherited, whereas interestingly, genes whose product involved in direct interaction with the environment (pstS) acquired by horizontal gene transfer. The substantial amino acid substitutions in PstS most likely contribute to the successful adaptation of bacteria in different ecological condition dealing with different phosphorus availability. The findings decipher the intelligence of the bacteria which enable them to carry out the targeted alteration of genes to cope up with the environmental condition.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aggarwal S, Somani VK, Bhatnagar R (2015) Phosphate starvation enhances the pathogenesis of Bacillus anthracis. Int J Med Microbiol 305:1–9. https://doi.org/10.1016/j.ijmm.2015.06.001
Aggarwal S, Somani VK, Gupta V et al (2017) Functional characterization of PhoPR two-component system and its implication in regulating phosphate homeostasis in Bacillus anthracis. Biochim Biophys Acta Gen Subj 1861:2956–2970. https://doi.org/10.1016/j.bbagen.2016.09.022
Anupama R, Mukherjee A, Babu S (2017) Gene-centric metagenome analysis reveals diversity of Pseudomonas aeruginosa biofilm gene orthologs in fresh water ecosystem. Genomics 110:1–10. https://doi.org/10.1016/j.ygeno.2017.08.010
Bohra V, Tikariha H, Dafale NA (2018) Genomically defined paenibacillus polymyxa ND24 for efficient cellulase production utilizing sugarcane bagasse as a substrate. Appl Biochem Biotechnol. https://doi.org/10.1007/s12010-018-2820-5
Braibant M, Lefèvre P, De Wit L et al (1996) Identification of a second Mycobacterium tuberculosis gene cluster encoding proteins of an ABC phosphate transporter. FEBS Lett 394:206–212. https://doi.org/10.1016/0014-5793(96)00953-2
Chekabab SM, Harel J, Dozois CM (2014a) Interplay between genetic regulation of phosphate homeostasis and bacterial virulence. Virulence 5:786–793. https://doi.org/10.4161/viru.29307
Chekabab SM, Jubelin G, Dozois CM, Harel J (2014b) PhoB activates Escherichia coli O157:H7 virulence factors in response to inorganic phosphate limitation. PLoS ONE 9:1–15. https://doi.org/10.1371/journal.pone.0094285
Cox GB, Webb D, Rosenberg H (1989) Specific Amino acid residues in both the PstB and PstC proteins are required for phosphate transport by the Escherichia coli Pst system. J Bacteriol 171:1531–1534. https://doi.org/10.1128/jb.171.3.1531-1534.1989
Crépin S, Chekabab SM, Le Bihan G et al (2011) The Pho regulon and the pathogenesis of Escherichia coli. Vet Microbiol 153:82–88. https://doi.org/10.1016/j.vetmic.2011.05.043
De Buck E, Maes L, Meyen E et al (2005) Legionella pneumophila Philadelphia-1 tatB and tatC affect intracellular replication and biofilm formation. Biochem Biophys Res Commun 331:1413–1420. https://doi.org/10.1016/j.bbrc.2005.04.060
Delgado S, Deutsch D, Sire JY (2017) Evolutionary analysis of the mammalian tuftelin sequence reveals features of functional importance. J Mol Evol 84:214–224. https://doi.org/10.1007/s00239-017-9789-5
Fiedler T, Mix M, Meyer U et al (2008) The two-component system PhoPR of Clostridium acetobutylicum is involved in phosphate-dependent gene regulation. J Bacteriol 190:6559–6567. https://doi.org/10.1128/JB.00574-08
Finn RD, Coggill P, Eberhardt RY et al (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44:D279–D285. https://doi.org/10.1093/nar/gkv1344
Finn RD, Attwood TK, Babbitt PC et al (2017) InterPro in 2017-beyond protein family and domain annotations. Nucleic Acids Res 45:190–199. https://doi.org/10.1093/nar/gkw1107
Ford JL, Gugger P, Wild SB, Mendz GL (2007) Phenylphosphonate transport by Helicobacter pylori. Helicobacter 12:609–615. https://doi.org/10.1111/j.1523-5378.2007.00550.x
Gaffé J, McKenzie C, Maharjan RP et al (2011) Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 72:398. https://doi.org/10.1007/s00239-011-9439-2
Gardner SG, Miller JB, Dean T et al (2015) Genetic analysis, structural modeling, and direct coupling analysis suggest a mechanism for phosphate signaling in Escherichia coli. BMC Genet 16:1–11. https://doi.org/10.1186/1471-2156-16-S2-S2
Gonzalez D, Richez M, Bergonzi C et al (2014) Crystal structure of the phosphate-binding protein (PBP-1) of an ABC-type phosphate transporter from Clostridium perfringens. Sci Rep 4:1–6. https://doi.org/10.1038/srep06636
Jehl P, Manguy J, Shields DC et al (2016) ProViz-a web-based visualization tool to investigate the functional and evolutionary features of protein sequences. Nucleic Acids Res 44:W11–W15. https://doi.org/10.1093/nar/gkw265
Jha V, Chande SP, Purohit HJ (2017) Seqestration options for phosphorus in wastewater. In: Purohit H, Kalia V, Vaidya A, Khardenavis A (eds) Optimization and applicability of bioprocesses. Springer, Singapore, pp 115–140. https://doi.org/10.1007/978-981-10-6863-8_6
Juhas M, Meer JR, Van Der Gaillard M et al (2009) Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiol 33:376–393. https://doi.org/10.1111/j.1574-6976.2008.00136.x
Karlin S (1996) Evolutionary conservation of RecA genes in relation to protein structure and function. these include : evolutionary conservation of RecA genes in relation to protein structure and function. J Bacteriol 178:1881–1894. https://doi.org/10.1128/jb.178.7.1881-1894.1996
Kearse M, Moir R, Wilson A et al (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kumwenda B, Litthauer D, Reva O (2014) Analysis of genomic rearrangements, horizontal gene transfer and role of plasmids in the evolution of industrial important Thermus species. BMC genomics 15:813. https://doi.org/10.1186/1471-2164-15-813
Lal S, Cheema S, Kalia VC (2008) Phylogeny vs genome reshuffling: horizontal gene transfer. Indian J Microbiol 48:228–242. https://doi.org/10.1007/s12088-008-0034-1
Lal S, Raje DV, Cheema S et al (2015) Investigating the phylogeny of hydrogen metabolism by comparative genomics: horizontal gene transfer. In: Kalia V (ed) Microbial factories. Springer, New Delhi, pp 317–345. https://doi.org/10.1007/978-81-322-2595-9_20
Lee SJ, Park YS, Kim SJ et al (2014) Crystal structure of PhoU from Pseudomonas aeruginosa, a negative regulator of the Pho regulon. J Struct Biol 188:22–29. https://doi.org/10.1016/j.jsb.2014.08.010
Liu J, Lou Y, Yokota H et al (2005) Crystal structure of a PhoU protein homologue: a new class of metalloprotein containing multinuclear iron clusters. J Biol Chem 280:15960–15966. https://doi.org/10.1074/jbc.M414117200
Makino K, Shinagawa H, Amemura M, Makata A (1986) Nucleotide sequence of the phoR gene, a regulatory gene for the phosphate regulon of Escherichia coli: homology between the PhoR and EnvZ proteins. JMolBiol 192:549–556
Martiny AC, Coleman ML, Chisholm SW (2006) Phosphate acquisition genes in Prochlorococcus ecotypes: evidence for genome-wide adaptation. Proc Natl Acad Sci USA 103:12552–12557. https://doi.org/10.1073/pnas.0601301103
Marzan LW, Shimizu K (2011) Metabolic regulation of Escherichia coli and its phoB and phoR genes knockout mutants under phosphate and nitrogen limitations as well as at acidic condition. Microb Cell Fact 10:1–15. https://doi.org/10.1186/1475-2859-10-39
Melese A, Gebrekidan H, Yli-halla M, Yitaferu B (2015) Phosphorus status, inorganic phosphorus forms, and other physicochemical properties of acid soils of Farta district, Northwestern highlands of Ethiopia. Appl Environ Soil Sci 2015:1–11. https://doi.org/10.1155/2015/748390
Meyers PR (2015) Analysis of recombinase A (recA/RecA) in the actinobacterial family Streptosporangiaceae and identification of molecular signatures. Syst Appl Microbiol 38:567–577. https://doi.org/10.1016/j.syapm.2015.10.001
Moreno-Letelier A, Olmedo G, Eguiarte LE et al (2011) Parallel evolution and horizontal gene transfer of the pst Operon in Firmicutes from oligotrophic environments. Int J Evol Biol 2011:1–10. https://doi.org/10.4061/2011/781642
Moussatova A, Kandt C, O’Mara ML, Tieleman DP (2008) ATP-binding cassette transporters in Escherichia coli. Biochim Biophys Acta 1778:1757–1771. https://doi.org/10.1016/j.bbamem.2008.06.009
Neves HI, Pereira TF, Yagil E, Spira B (2015) Ugp and PitA participate in the selection of PHO-constitutive mutants. J Bacteriol 197:1378–1385. https://doi.org/10.1128/JB.02566-14
Ortega C, Mancera G, Enríquez R et al (2016) First identification of Francisella noatunensis subsp. orientalis causing mortality in mexican tilapia Oreochromis spp.. Dis Aquat Organ 120:205–215. https://doi.org/10.3354/dao02999
Oswald C, Holland IB, Schmitt L (2006) The motor domains of ABC-transporters: what can structures tell us? Naunyn Schmiedebergs Arch Pharmacol 372:385–399. https://doi.org/10.1007/s00210-005-0031-4
Paquola ACM, Asif H, Pereira CAB et al (2018) Horizontal gene transfer building prokaryote genomes: genes related to exchange between cell and environment are frequently transferred. J Mol Evol 86:190–203. https://doi.org/10.1007/s00239-018-9836-x
Pegos VR, Hey L, Lamirande J et al (2017) Phosphate-binding protein from Polaromonas JS666: Purification, characterization, crystallization and sulfur SAD phasing. Acta Crystallogr Sect Struct Biol Commun 73:342–346. https://doi.org/10.1107/S2053230X17007373
Pylro VS, Vespoli L, de S, Duarte, Yotoko GF KSC (2012) Detection of horizontal gene transfers from phylogenetic comparisons. Int J Evol Biol 2012:1–7. https://doi.org/10.1155/2012/813015
Raeside C, Gaffé J, Deatherage DE et al (2014) Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. MBio 5:e01377–e01314. https://doi.org/10.1128/mBio.01377-14
Salzberg LI, Botella E, Hokamp K et al (2015) Genome-wide analysis of phosphorylated PhoP binding to chromosomal DNA reveals several novel features of the PhoPR-mediated phosphate limitation response in Bacillus subtilis. J Bacteriol 197:1492–1506. https://doi.org/10.1128/JB.02570-14
Santos-Beneit F (2015) The Pho regulon: a huge regulatory network in bacteria. Front Microbiol 6:1–13. https://doi.org/10.3389/fmicb.2015.00402
Sola-Landa a, Moura RS, Martín JF (2003) The two-component PhoR-PhoP system controls both primary metabolism and secondary metabolite biosynthesis in Streptomyces lividans. Proc Natl Acad Sci USA 100:6133–6138. https://doi.org/10.1073/pnas.0931429100
Suyama M, Bork P (2001) Evolution of prokaryotic gene order: genome rearrangements in closely related species. Trends Genet 17:10–13
Takemaru KI, Mizuno M, Kobayashi Y (1996) A Bacillus subtilis gene cluster similar to the Escherichia coli phosphate-specific transport (pst) operon: Evidence for a tandemly arranged pstB gene. Microbiology 142:2017–2020. https://doi.org/10.1099/13500872-142-8-2017
Tamames J, Sánchez PD, Nikel PI, Pedrós-alió C (2016) Quantifying the relative importance of phylogeny and environmental preferences as drivers of gene content in prokaryotic microorganisms. Front Microbiol 7:1–12. https://doi.org/10.3389/fmicb.2016.00433
Tanabe M, Mirza O, Bertrand T et al (2007) Structures of OppA and PstS from Yersinia pestis indicate variability of interactions with transmembrane domains. Acta Crystallogr D Biol Crystallogr 63:1185–1193. https://doi.org/10.1107/S0907444907048299
Tiessen H (2011) Phosphorus availability in the environment. In: eLS. Wiley, New York. http://www.els.net https://doi.org/10.1002/9780470015902.a0003188.pub2. Accessed 30 September 2018
Ullastres A, Merenciano M, Guio L, González J (2016) Transposable elements: a toolkit for stress and environmental adaptation in bacteria. In: de Bruijn F (ed) Stress and environmental regulation of gene expression and adaptation in bacteria, I & II. Wiley, pp137–145. https://doi.org/10.1002/9781119004813.ch11
V’yugin VV, Gelfand MS, Lyubetsky VA (2003) Identification of horizontal gene transfer from phylogenetic gene trees. Mol Biol 37:571–584. https://doi.org/10.1023/A:1025191411933
Vershinina OA, Znamenskaya LV (2002) The Pho regulons of bacteria. Microbiology 71:497–511. https://doi.org/10.1023/A:1020547616096
Webb DC, Rosenberg H, Cox GB (1992) Mutational analysis of the Escherichia coli phosphate-specific transport system, a member of the traffic ATPase (or ABC) family of membrane transporters. A role for proline residues in transmembrane helices. J Biol Chem 267:24661–24668. https://doi.org/10.1111/j.1749-6632.1956.tb40107.x
Wu X, Liu L, Zhang Z et al (2014) Phylogenetic and genetic characterization of Acidithiobacillus strains isolated from different environments. World J Microbiol Biotechnol 30:3197–3209. https://doi.org/10.1007/s11274-014-1747-4
Yang Z (1996) Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol Evol 11:367–372. https://doi.org/10.1016/0169-5347(96)10041-0
Yang K, Wang M, Metcalf WW (2009) Uptake of glycerol-2-phosphate via the ugp-encoded transporter in Escherichia coli K-12. J Bacteriol 191:4667–4670. https://doi.org/10.1128/JB.00235-09
Acknowledgements
Varsha Jha and Hitesh Tikariha are grateful to University Grant Commision (UGC) for Senior Research Fellowship (SRF) and also acknowledge the Director, CSIR-National Environmental Engineering Research Institute (CSIR-NEERI) for providing facilities for this work [KRC manuscript no.: CSIR-NEERI/KRC/2018/FEB/EBGD/2].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Jha, V., Tikariha, H., Dafale, N.A. et al. Exploring the rearrangement of sensory intelligence in proteobacteria: insight of Pho regulon. World J Microbiol Biotechnol 34, 172 (2018). https://doi.org/10.1007/s11274-018-2551-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11274-018-2551-3