1887

Abstract

Hierarchical utilization of substrate by microbes (utilization of simple carbon sources prior to complex ones) poses a major limitation to the efficient remediation of aromatic pollutants. Aromatic compounds, being complex and reduced in nature, appear to be a deferred choice as the carbon source in the presence of a plethora of simple organic compounds in the environment. The soil bacterium CSV86 displays a unique carbon source utilization hierarchy. It preferentially utilizes aromatics over glucose and co-metabolizes them with succinate or pyruvate (Basu ., 2006, , 72 : 22226–2230). In the present study, the substrate utilization hierarchy for strain CSV86 was tested for additional simple carbon sources such as glycerol, acetate, and tri-carboxylic acid (TCA) cycle intermediates like α-ketoglutarate and fumarate. When grown on a mixture of aromatics (benzoate or naphthalene) plus glycerol, the strain displayed a diauxic growth profile with significantly high activity of aromatic utilization enzymes (catechol 1,2- or 2,3-dioxygenase, respectively) in the first-log phase. This suggests utilization of aromatics in the first-log phase followed by glycerol in the second-log phase. On a mixture of an aromatic plus organic acid (acetate, α-ketoglutarate or fumarate), the strain displayed a monoauxic growth profile, indicating co-metabolism. Interestingly, the presence of glycerol, acetate, α-ketoglutarate or fumarate does not repress metabolism/utilization of the aromatic. Thus, the substrate utilization hierarchy of strain CSV86 is aromatics=organic acids>glucose/glycerol, which is unique as compared to other species, where degradation of aromatics is repressed by glycerol, glucose, acetate or organic acids, including TCA cycle intermediates. This novel substrate utilization hierarchy appears to be a global metabolic phenomenon in strain CSV86, thus implying it to be an ideal host for metabolic engineering as well as for its potential application in bioremediation.

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/content/journal/micro/10.1099/mic.0.001206
2022-08-04
2022-08-17
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References

  1. Boström C-E, Gerde P, Hanberg A, Jernström B, Johansson C et al. Cancer risk assessment, indicators, and guidelines for polycyclic aromatic hydrocarbons in the ambient air. Environ Health Perspect 2002; 110 Suppl 3:451–488 [View Article] [PubMed]
    [Google Scholar]
  2. Choi H, Jedrychowski W, Spengler J, Camann DE, Whyatt RM et al. International studies of prenatal exposure to polycyclic aromatic hydrocarbons and fetal growth. Environ Health Perspect 2006; 114:1744–1750 [View Article] [PubMed]
    [Google Scholar]
  3. Görke B, Stülke J. Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 2008; 6:613–624 [View Article] [PubMed]
    [Google Scholar]
  4. Holtel A, Marqués S, Möhler I, Jakubzik U, Timmis KN. Carbon source-dependent inhibition of xyl operon expression of the Pseudomonas putida TOL plasmid. J Bacteriol 1994; 176:1773–1776 [View Article] [PubMed]
    [Google Scholar]
  5. Rojo F. Carbon catabolite repression in Pseudomonas : optimizing metabolic versatility and interactions with the environment. FEMS Microbiol Rev 2010; 34:658–684 [View Article] [PubMed]
    [Google Scholar]
  6. Monod J. The growth of bacterial cultures. Annu Rev Microbiol 1949; 3:371–394 [View Article]
    [Google Scholar]
  7. Mohapatra B, Phale PS. Microbial degradation of naphthalene and substituted naphthalenes: metabolic diversity and genomic insight for bioremediation. Front Bioeng Biotechnol 2021; 9:144 [View Article] [PubMed]
    [Google Scholar]
  8. Seo JS, Keum YS, Li QX. Bacterial degradation of aromatic compounds. Int J Environ Res Public Health 2009; 6:278–309 [View Article] [PubMed]
    [Google Scholar]
  9. Park H, McGill SL, Arnold AD, Carlson RP. Pseudomonad reverse carbon catabolite repression, interspecies metabolite exchange, and consortial division of labor. Cell Mol Life Sci 2020; 77:395–413 [View Article] [PubMed]
    [Google Scholar]
  10. Mahajan MC, Phale PS, Vaidyanathan CS. Evidence for the involvement of multiple pathways in the biodegradation of 1- and 2-methylnaphthalene by Pseudomonas putida CSV86. Arch Microbiol 1994; 161:425–433 [View Article] [PubMed]
    [Google Scholar]
  11. Mohapatra B, Nain S, Sharma R, Phale PS. Functional genome mining and taxono‐genomics reveal eco‐physiological traits and species distinctiveness of aromatic‐degrading Pseudomonas bharatica sp. nov. Environ Microbiol Rep 2022; 14:464–474 [View Article] [PubMed]
    [Google Scholar]
  12. Basu A, Apte SK, Phale PS. Preferential utilization of aromatic compounds over glucose by Pseudomonas putida CSV86. Appl Environ Microbiol 2006; 72:2226–2230 [View Article] [PubMed]
    [Google Scholar]
  13. Karishma M, Trivedi VD, Choudhary A, Mhatre A, Kambli P et al. Analysis of preference for carbon source utilization among three strains of aromatic compounds degrading Pseudomonas. FEMS Microbiol Lett 2015; 362:fnv139 [View Article] [PubMed]
    [Google Scholar]
  14. Phale PS, Mohapatra B, Malhotra H, Shah BA. Eco-physiological portrait of a novel Pseudomonas sp. CSV86: an ideal host/candidate for metabolic engineering and bioremediation. Environ Microbiol 2022; 24:2797–2816 [View Article] [PubMed]
    [Google Scholar]
  15. Shrivastava R, Purohit H, S Phale P. Metabolism and preferential utilization of phenylacetic acid and 4-hydroxyphenylacetic acid in Pseudomonas putida CSV86. J Bioremed Biodegrad 2011; 02:2 [View Article]
    [Google Scholar]
  16. Basu A, Phale PS. Inducible uptake and metabolism of glucose by the phosphorylative pathway in Pseudomonas putida CSV86. FEMS Microbiol Lett 2006; 259:311–316 [View Article] [PubMed]
    [Google Scholar]
  17. Basu A, Shrivastava R, Basu B, Apte SK, Phale PS. Modulation of glucose transport causes preferential utilization of aromatic compounds in Pseudomonas putida CSV86. J Bacteriol 2007; 189:7556–7562 [View Article] [PubMed]
    [Google Scholar]
  18. Choudhary A, Modak A, Apte SK, Phale PS. Transcriptional modulation of transport- and metabolism-associated gene clusters leading to utilization of Benzoate in preference to glucose in Pseudomonas putida CSV86. Appl Environ Microbiol 2017; 83:e01280-17 [View Article] [PubMed]
    [Google Scholar]
  19. Basu A, Dixit SS, Phale PS. Metabolism of benzyl alcohol via catechol ortho-pathway in methylnaphthalene-degrading Pseudomonas putida CSV86. Appl Microbiol Biotechnol 2003; 62:579–585 [View Article] [PubMed]
    [Google Scholar]
  20. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72:248–254 [View Article] [PubMed]
    [Google Scholar]
  21. Nikel PI, Romero-Campero FJ, Zeidman JA, Goñi-Moreno Á, de Lorenzo V. The glycerol-dependent metabolic persistence of Pseudomonas putida KT2440 reflects the regulatory logic of the GlpR repressor. mBio 2015; 6:e00340-15 [View Article] [PubMed]
    [Google Scholar]
  22. Chaparro JM, Badri DV, Bakker MG, Sugiyama A, Manter DK et al. Root exudation of phytochemicals in Arabidopsis follows specific patterns that are developmentally programmed and correlate with soil microbial functions. PLoS ONE 2013; 8:e55731 [View Article] [PubMed]
    [Google Scholar]
  23. Ohtsubo Y, Goto H, Nagata Y, Kudo T, Tsuda M. Identification of a response regulator gene for catabolite control from a PCB-degrading beta-proteobacteria, Acidovorax sp. KKS102. Mol Microbiol 2006; 60:1563–1575 [View Article] [PubMed]
    [Google Scholar]
  24. Shourian M, Noghabi KA, Zahiri HS, Bagheri T, Karbalaei R et al. Efficient phenol degradation by a newly characterized pseudomonas sp. SA01 isolated from pharmaceutical wastewaters. Desalination 2009; 246:577–594
    [Google Scholar]
  25. Chen BY, Chen WM, Chang JS. Optimal biostimulation strategy for phenol degradation with indigenous rhizobium Ralstonia taiwanensis. J Hazard Mater 2007; 139:232–237 [View Article] [PubMed]
    [Google Scholar]
  26. Samson R, Beaumier D, Beaulieu C. Simultaneous evaluation of on-line microcalorimetry and fluorometry during batch culture of Pseudomonas putida-ATCC 11172 and Saccharomyces cerevisiae ATCC 18824. J Biotechnol 1987; 6:175–190 [View Article] [PubMed]
    [Google Scholar]
  27. Santos PM, Blatny JM, Di Bartolo I, Valla S, Zennaro E. Physiological analysis of the expression of the styrene degradation gene cluster in Pseudomonas fluorescens ST. Appl Environ Microbiol 2000; 66:1305–1310 [View Article] [PubMed]
    [Google Scholar]
  28. Choudhary A, Purohit H, Phale PS. Benzoate transport in Pseudomonas putida CSV86. FEMS Microbiol Lett 2017; 364:364 [View Article] [PubMed]
    [Google Scholar]
  29. Heiman AS, Cooper WT. Solid-state 13C nuclear magnetic resonance spectroscopy of simultaneously metabolized acetate and phenol in a soil Pseudomonas sp. Appl Environ Microbiol 1987; 53:156–162 [View Article] [PubMed]
    [Google Scholar]
  30. Schmidt SK, Alexander M. Effects of dissolved organic carbon and second substrates on the biodegradation of organic compounds at low concentrations. Appl Environ Microbiol 1985; 49:822–827 [View Article] [PubMed]
    [Google Scholar]
  31. Dal S, Steiner I, Gerischer U. Multiple operons connected with catabolism of aromatic compounds in Acinetobacter sp. strain ADP1 are under carbon catabolite repression. J Mol Microbiol Biotechnol 2002; 4:389–404
    [Google Scholar]
  32. Fischer R, Bleichrodt FS, Gerischer UC. Aromatic degradative pathways in Acinetobacter baylyi underlie carbon catabolite repression. Microbiology (Reading) 2008; 154:3095–3103 [View Article] [PubMed]
    [Google Scholar]
  33. Hughes EJ, Bayly RC. Control of catechol meta-cleavage pathway in Alcaligenes eutrophus. J Bacteriol 1983; 154:1363–1370 [View Article] [PubMed]
    [Google Scholar]
  34. Müller C, Petruschka L, Cuypers H, Burchhardt G, Herrmann H. Carbon catabolite repression of phenol degradation in Pseudomonas putida is mediated by the inhibition of the activator protein PhlR. J Bacteriol 1996; 178:2030–2036 [View Article] [PubMed]
    [Google Scholar]
  35. Badri DV, Vivanco JM. Regulation and function of root exudates. Plant Cell Environ 2009; 32:666–681 [View Article] [PubMed]
    [Google Scholar]
  36. Collier DN, Hager PW, Phibbs PV Jr. Catabolite repression control in the Pseudomonads. Res Microbiol 1996; 147:551–561 [View Article] [PubMed]
    [Google Scholar]
  37. Duetz WA, Marqués S, de Jong C, Ramos JL, van Andel JG. Inducibility of the TOL catabolic pathway in Pseudomonas putida (pWW0) growing on succinate in continuous culture: evidence of carbon catabolite repression control. J Bacteriol 1994; 176:2354–2361 [View Article] [PubMed]
    [Google Scholar]
  38. McFall SM, Abraham B, Narsolis CG, Chakrabarty AM. A tricarboxylic acid cycle intermediate regulating transcription of a chloroaromatic biodegradative pathway: fumarate-mediated repression of the clcABD operon. J Bacteriol 1997; 179:6729–6735 [View Article] [PubMed]
    [Google Scholar]
  39. Ampe F, Léonard D, Lindley ND. Repression of phenol catabolism by organic acids in Ralstonia eutropha. Appl Environ Microbiol 1998; 64:1–6 [View Article]
    [Google Scholar]
  40. Brzostowicz PC, Reams AB, Clark TJ, Neidle EL. Transcriptional cross-regulation of the catechol and protocatechuate branches of the β-Ketoadipate pathway contributes to carbon source-dependent expression of the Acinetobacter sp. strain ADP1 pobA gene. Appl Environ Microbiol 2003; 69:1598–1606 [View Article] [PubMed]
    [Google Scholar]
  41. Choi KY, Zylstra GJ, Kim E. Benzoate catabolite repression of the phthalate degradation pathway in Rhodococcus sp. strain DK17. Appl Environ Microbiol 2007; 73:1370–1374 [View Article] [PubMed]
    [Google Scholar]
  42. Donoso RA, Pérez-Pantoja D, González B. Strict and direct transcriptional repression of the pobA gene by benzoate avoids 4-hydroxybenzoate degradation in the pollutant degrader bacterium Cupriavidus necator JMP134. Environ Microbiol 2011; 13:1590–1600 [View Article] [PubMed]
    [Google Scholar]
  43. Heinaru E, Viggor S, Vedler E, Truu J, Merimaa M et al. Reversible accumulation of p-hydroxybenzoate and catechol determines the sequential decomposition of phenolic compounds in mixed substrate cultivations in pseudomonads. FEMS Microbiol Ecol 2001; 37:79–89 [View Article]
    [Google Scholar]
  44. Reardon KF, Mosteller DC, Rogers JB, DuTeau NM, Kim KH. Biodegradation kinetics of aromatic hydrocarbon mixtures by pure and mixed bacterial cultures. Environ Health Perspect 2002; 110 Suppl 6:1005–1011 [View Article] [PubMed]
    [Google Scholar]
  45. Bateman JN, Speer B, Feduik LI, Hartline RA. Naphthalene association and uptake in Pseudomonas putida. J Bacteriol 1986; 166:155–161 [View Article] [PubMed]
    [Google Scholar]
  46. Mrozik A, Łabużek S, Piotrowska-Seget Z. Changes in fatty acid composition in Pseudomonas putida and Pseudomonas stutzeri during naphthalene degradation. Microbiol Res 2005; 160:149–157 [View Article] [PubMed]
    [Google Scholar]
  47. Mazzoli R, Pessione E, Giuffrida MG, Fattori P, Barello C et al. Degradation of aromatic compounds by Acinetobacter radioresistens S13: growth characteristics on single substrates and mixtures. Arch Microbiol 2007; 188:55–68 [View Article] [PubMed]
    [Google Scholar]
  48. Thayer JR, Wheelis ML. Characterization of a benzoate permease mutant of Pseudomonas putida. Arch Microbiol 1976; 110:37–42 [View Article] [PubMed]
    [Google Scholar]
  49. Yuroff AS, Sabat G, Hickey WJ. Transporter-mediated uptake of 2-chloro- and 2-hydroxybenzoate by Pseudomonas huttiensis strain D1. Appl Environ Microbiol 2003; 69:7401–7408 [View Article] [PubMed]
    [Google Scholar]
  50. Paliwal V, Raju SC, Modak A, Phale PS, Purohit HJ. Pseudomonas putida CSV86: a candidate genome for genetic bioaugmentation. PLoS One 2014; 9:e84000 [View Article] [PubMed]
    [Google Scholar]
  51. Pernstich C, Senior L, MacInnes KA, Forsaith M, Curnow P. Expression, purification and reconstitution of the 4-hydroxybenzoate transporter PcaK from Acinetobacter sp. ADP1. Protein Expr Purif 2014; 101:68–75 [View Article] [PubMed]
    [Google Scholar]
  52. Basu A, Phale PS. Conjugative transfer of preferential utilization of aromatic compounds from Pseudomonas putida CSV86. Biodegradation 2008; 19:83–92 [View Article] [PubMed]
    [Google Scholar]
  53. Phale PS, Shah BA, Malhotra H. Variability in assembly of degradation operons for naphthalene and its derivative, carbaryl, suggests mobilization through horizontal gene transfer. Genes (Basel) 2019; 10:569 [View Article] [PubMed]
    [Google Scholar]
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