Abstract
Pseudomonas sp. strain C7 isolated from sediment of Thane creek near Mumbai, India, showed the ability to grow on glucose and carbaryl in the presence of 7.5 and 3.5% of NaCl, respectively. It also showed good growth in the absence of NaCl indicating the strain to be halotolerant. Increasing salt concentration impacted the growth on carbaryl; however, the specific activity of various enzymes involved in the metabolism remained unaffected. Among various enzymes, 1-naphthol 2-hydroxylase was found to be sensitive to chloride as compared to carbaryl hydrolase and gentisate 1,2-dioxygenase. The intracellular concentration of Cl− ions remained constant (6–8 mM) for cells grown on carbaryl either in the presence or absence of NaCl. Thus the ability to adapt to the increasing concentration of NaCl is probably by employing chloride efflux pump and/or increase in the concentration of osmolytes as mechanism for halotolerance. The halotolerant nature of the strain will be beneficial to remediate carbaryl from saline agriculture fields, ecosystems and wastewaters.
Similar content being viewed by others
Abbreviations
- CH:
-
Carbaryl hydrolase
- 1NH:
-
1-Naphthol 2-hydroxylase
- GDO:
-
Gentisate dioxygenase
- C23DO:
-
Catechol 2,3-dioxygenase
- PDO:
-
Protocatechuate 3,4-dioxygenase
References
Arulazhagan P, Vasudevan N (2011) Biodegradation of polycyclic aromatic hydrocarbons by a halotolerant bacterial strain Ochrobactrum sp. VA1. Mar Pollut Bull 62:388–394
Arulazhagan P, Vasudevan N, Yeom IT (2010) Biodegradation of polycyclic aromatic hydrocarbon by bacterial consortium isolated from marine environment. Int J Environ Sci Tech 7:639–652
Bastos AE, Moon DH, Rossi A, Trevors JT, Tsai SM (2000) Salt-tolerant phenol-degrading microorganisms isolated from Amazonian soil samples. Arch Microbiol 174:346–352
Bedard DL, Wagner RE, Brennan MJ, Haberl ML, Brown JF Jr (1987) Extensive degradation of Aroclors and environmentally transformed polychlorinated biphenyls by Alcaligenes eutrophus H850. Appl Environ Microbiol 53:1094–1102
Berlendis S, Cayol JL, Verhe F, Laveau S, Tholozan JL, Ollivier B, Auria R (2010) First evidence of aerobic biodegradation of BTEX compounds by pure cultures of Marinobacter. Appl Biochem Biotechnol 160:1992–1999
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Chapalmadugu S, Chaudhry GR (1993) Isolation of a constitutively expressed enzyme for hydrolysis of carbaryl in Pseudomonas aeruginosa. J Bacteriol 175:6711–6716
Ciulla RA, Diaz MR, Taylor BF, Roberts MF (1997) Organic osmolytes in aerobic bacteria from mono lake, an alkaline, moderately hypersaline environment. Appl Environ Microbiol 63:220–226
Crawford RL, McCoy E, Harkin JM, Kirk TK, Obst JR (1973) Degradation of methoxylated benzoic acids by a Nocardia from a lignin-rich environment: significance to lignin degradation and effect of chloro substituents. Appl Microbiol 26:176–184
Dalvi S, Azetsu S, Patrauchan MA, Aktas DF, Fathepure BZ (2012) Proteogenomic elucidation of the initial steps in the benzene degradation pathway of a novel halophile, Arhodomonas sp. strain Rozel, isolated from a hypersaline environment. Appl Environ Microbiol 8:7309–7316
Dalvi S, Youssef NH, Fathepure BZ (2016) Microbial community structure analysis of a benzoate-degrading halophilic archaeal enrichment. Extremophiles 20:311–321
de Carvalho CC, da Fonseca MM (2005) Degradation of hydrocarbons and alcohols at different temperatures and salinities by Rhodococcus erythropolis DCL14. FEMS Microbiol Ecol 51:389–399
Fathepure BZ (2014) Recent studies in microbial degradation of petroleum hydrocarbons in hypersaline environments. Front Microbiol 5:173
Feng TC, Cui CZ, Dong F, Feng YY, Liu YD, Yang XM (2012) Phenanthrene biodegradation by halophilic Martelella sp. AD-3. J Appl Microbiol 113:779–789
Fujisawa H, Hayashi O (1968) Protocatechuate 3,4-dioxygenase. I. Crystallization and characterization. J Biol Chem 243:2673–2681
Galinski E, Truper H (1994) Microbial behavior in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108
Garcia MT, Mellado E, Ostos JC, Ventosa A (2004) Halomonas organivorans sp. nov., a moderate halophile able to degrade aromatic compounds. Int J Syst Evol Microbiol 54:1723–1728
Guo G, Fang T, Wang C, Huang Y, Tian F, Cui Q, Wang H (2015) Isolation and characterization of two novel halotolerant catechol 2,3-dioxygenases from a halophilic bacterial consortium. Sci Rep 5:17603
Hansen JB, Olsen RH (1978) Isolation of large bacterial plasmids and characterization of the P2 incompatibility group plasmids pMG1 and pMG5. J Bacteriol 135:227–238
Hodkinson B, Lutzoni F (2009) A microbiotic survey of lichen-associated bacteria reveals a new lineage from the Rhizobiales. Symbiosis 49:163–180
Huang L, Hu H, Tang H, Liu Y, Xu P, Shi J, Lin K, Luo Q, Cui C (2015) Identification and characterization of a novel gentisate 1,2-dioxygenase gene from a halophilic Martelella strain. Sci Rep 5:14307
Imhoff JF, Rodriguez-Valera F (1984) Betaine is the main compatible solute of halophilic eubacteria. J Bacteriol 160:478–479
Jencova V, Strnad H, Chodora Z, Ulbrich P, Vlcek C, Hickey WJ, Paces V (2008) Nucleotide sequence, organization and characterization of the (halo)aromatic acid catabolic plasmid pA81 from Achromobacter xylosoxidans A8. Res Microbiol 159:118–127
Kendrick PN, Trim AJ, Atwal JK, Brown PM (1991) Direct gas chromatographic determination of carbaryl residues in honeybees (Apis mellifera L.) using a nitrogen-phosphorus detector with confirmation by formation of a chemical derivative. Bull Environ Contam Toxicol 46:654–661
Killham K, Firestone MK (1984) Salt stress control of intracellular solutes in Streptomycetes indigenous to saline soils. Appl Environ Microbiol 47:301–306
Kim OS, Cho YJ, Lee K, Yoon SH, Kim M, Na H, Park SC, Jeon YS, Lee JH, Yi H, Won S, Chun J (2012) Introducing EzTaxon-e: a prokaryotic 16 S rRNA gene sequence database with phylotypes that represent uncultured species. Int J Syst Evol Microbiol 62:716–721
Kojima Y, Fujisawa H, Nakazawa A, Nakazawa T, Kanetsuna F, Taniuchi H, Nozaki M, Hayaishi O (1967) Studies on pyrocatechase. I. Purification and spectral properties. J Biol Chem 242:3270–3278
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Larkin MJ, Day MJ (1986) The metabolism of carbaryl by three bacterial isolates, Pseudomonas spp. (NCIB 12042 & 12043) and Rhodococcus sp. (NCIB 12038) from garden soil. J Appl Bacteriol 60:233–242
Mazzoli R, Pessione E, Giuffrida MG, Fattori P, Barello C, Giunta C, Lindley ND (2007) Degradation of aromatic compounds by Acinetobacter radioresistens S13: growth characteristics on single substrates and mixtures. Arch Microbiol 188:55–68
Megharaj M, Venkateswarlu K, Naidu R (2011) Effects of carbaryl and 1-naphthol on soil population of cyanobacteria and microalgae and select cultures of diazotrophic cyanobacteria. Bull Environ Contam Toxicol 87:324–329
Mille G, Almallah M, Bianchi M, Wambeke F, Bertrand JC (1991) Effect of salinity on petroleum biodegradation. Fresenius J. Anal Chem 339:788–791
Mostert MA, Schoeman AS, van der Merwe M (2002) The relative toxicities of insecticides to earthworms of the Pheretima group (Oligochaeta). Pest Manag Sci 58:446–450
Müller V, Oren A (2003) Metabolism of chloride in halophilic prokaryotes. Extremophiles 7:261–266
Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biotechnol 28:56–63
Pires RF, Franco MR Jr (2012) Solubility of salicylic acid in water + salt (NaCl, KCl, NaBr, Na2SO4 and K2SO4) at 293.5–313.3 K. Fluid Phase Equilib 330:48–51
Ren L, Shi Y, Jia Y, Yan Y (2015) Genome sequence of Arthrobacter sp. YC-RL1, an aromatic compound-degrading bacterium. Genome Announc 3. doi:10.1128/genomeA.00749-15.
Roberts MF (2005) Organic compatible solutes of halotolerant and halophilic microorganisms. Saline Syst 1:5
Saab J, Naccoul RA, Stephan J, Goutaudier C, Ouaini R, Mokbel I, Ouaini N, Jose J (2009) Mass transfer of carbaryl from pure water to salt aqueous solution: result comparison between sea and lab-made water. Water Air Soil Pollut 209:241–249
Saum SH, Müller V (2007) Salinity-dependent switching of osmolyte strategies in a moderately halophilic bacterium: glutamate induces proline biosynthesis in Halobacillus halophilus. J Bacteriol 189:6968–6975
Saum SH, Müller V (2008) Regulation of osmoadaptation in the moderate halophile Halobacillus halophilus: chloride, glutamate and switching osmolyte strategies. Saline Syst 4:4
Saum SH, Pfeiffer F, Palm P, Rampp M, Schuster SC, Muller V, Oesterhelt D (2013) Chloride and organic osmolytes: a hybrid strategy to cope with elevated salinities by the moderately halophilic, chloride-dependent bacterium Halobacillus halophilus. Environ Microbiol 15:1619–1633
Schultz SG, Wilson NL, Epstein W (1962) Cation transport in Escherichia coli. II. Intracellular chloride concentration. J Gen Physiol 46:159–166
Schwarz FP (1977) Determination of temperature dependence of solubilities of polycyclic aromatic hydrocarbons in aqueous solutions by a fluorescence method. J Chem Eng Data 22:273–277
Singh R, Trivedi VD, Phale PS (2013) Metabolic regulation and chromosomal localization of carbaryl degradation pathway in Pseudomonas sp. strains C4, C5 and C6. Arch Microbiol 195:521–535
Smulders CJ, Bueters TJ, Van Kleef RG, Vijverberg HP (2003) Selective effects of carbamate pesticides on rat neuronal nicotinic acetylcholine receptors and rat brain acetylcholinesterase. Toxicol Appl Pharmacol 193:139–146
Stanier RY, Ingraham JL (1954) Protocatechuic acid oxidase. J Biol Chem 210:799–808
Suarez M, Ferrer E, Garrido-Pertierra A (1995) Purification and characterization of the 3-hydroxybenzoate-6-hydroxylase from Klebsiella pneumoniae. FEMS Microbiol Lett 126:283–290
Swetha VP, Phale PS (2005) Metabolism of carbaryl via 1,2-dihydroxynaphthalene by soil isolates Pseudomonas sp. strains C4, C5, and C6. Appl Environ Microbiol 71:5951–5956
SwethaVP, Basu A, Phale PS (2007) Purification and characterization of 1-naphthol-2-hydroxylase from carbaryl-degrading Pseudomonas strain C4. J Bacteriol 189:2660–2666
Ventosa A, Nieto JJ, Oren A (1998) Biology of moderately halophilic aerobic bacteria. Microbiol Mol Biol Rev 62:504–544
Vreeland RH (1987) Mechanisms of halotolerance in microorganisms. Crit Rev Microbiol 14:311–356
You Y, Shim J, Cho CH, Ryu MH, Shea PJ, Kamala-Kannan S, Chae JC, Oh BT (2013) Biodegradation of BTEX mixture by Pseudomonas putida YNS1 isolated from oil-contaminated soil. J Basic Microbiol 53:469–475
Zhao B, Wang H, Mao X, Li R (2009) Biodegradation of phenanthrene by a halophilic bacterial consortium under aerobic conditions. Curr Microbiol 58:205–210
Acknowledgements
VDT acknowledges CSIR, Govt. of India for senior research fellowship, AB and MV to IIT-B for IRCC internship, KG to IIT-B for teaching assistantship. PP acknowledges research grant from Board of Research in Nuclear Sciences, Govt. of India, India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Matthias Boll.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Trivedi, V.D., Bharadwaj, A., Varunjikar, M.S. et al. Insights into metabolism and sodium chloride adaptability of carbaryl degrading halotolerant Pseudomonas sp. strain C7. Arch Microbiol 199, 907–916 (2017). https://doi.org/10.1007/s00203-017-1363-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00203-017-1363-4