Simultaneous Catabolism of Plant-Derived Aromatic Compounds Results in Enhanced Growth for Members of the Roseobacter Lineage

Applied and Environmental Microbiology

Volumn 79, Issue 12, 2013, Pages 3716-3723

  Gulvik, Christopher A ^a   Buchan, Alison ^a  

^a UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON CONCENTRATIONS; DISSOLVED ORGANIC CARBON; EQUIMOLAR CONCENTRATIONS; GROWTH SUBSTRATES; METABOLIC VERSATILITY; SUBSTRATE CONCENTRATIONS; SUBSTRATE UTILIZATION; TRANSCRIPTIONAL REGULATION;

AROMATIZATION; BACTERIA; CARBON; METABOLISM; WETLANDS;

SUBSTRATES;

4 HYDROXYBENZOIC ACID; 4 HYDROXYBENZOIC ACID ESTER; 4-HYDROXYBENZOIC ACID; ACYL COENZYME A; AROMATIC HYDROCARBON; BENZOIC ACID DERIVATIVE; BENZOYL COENZYME A; BENZOYL-COENZYME A; HYDROXYBENZOIC ACID DERIVATIVE; PROTOCATECHUATE 3,4 DIOXYGENASE; PROTOCATECHUIC ACID;

AROMATIC HYDROCARBON; CARBON CYCLE; CATABOLISM; CONCENTRATION (COMPOSITION); DISSOLVED ORGANIC CARBON; ENZYME ACTIVITY; GROWTH RATE; HIERARCHICAL SYSTEM; MICROBIAL COMMUNITY; PLANT COMMUNITY; SALTMARSH; SOIL MICROORGANISM; SUBSTRATE;

ARTICLE; BIOLOGY; CARBON CYCLE; GROWTH, DEVELOPMENT AND AGING; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ROSEOBACTER; SEDIMENT; ULTRAVIOLET SPECTROPHOTOMETRY; WETLAND;

ACYL COENZYME A; BENZOATES; CARBON CYCLE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTATIONAL BIOLOGY; GEOLOGIC SEDIMENTS; HYDROCARBONS, AROMATIC; HYDROXYBENZOATES; METABOLIC NETWORKS AND PATHWAYS; PARABENS; PROTOCATECHUATE-3,4-DIOXYGENASE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; ROSEOBACTER; SPECTROPHOTOMETRY, ULTRAVIOLET; WETLANDS;

ROSEOBACTER; RUEGERIA; SAGITTULA STELLATA;

EID: 84878608360     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00405-13     Document Type: Article

References (65)

1. Wang Y, Yang J, Lee OO, Dash S, Lau SCK, Al-Suwailem A, Wong TYH, Danchin A, Qian P-Y. 2011. Hydrothermally generated aromatic compounds are consumed by bacteria colonizing in Atlantis II Deep of the Red Sea. ISME J. 5:1652-1659.
2. Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annu. Rev. Plant Biol. 54:519-546.
3. Higuchi T. 1990. Lignin biochemistry: biosynthesis and biodegradation. Wood Sci. Technol. 24:23-63.
4. Wakeham SG, Schaffner C, Giger W. 1980. Polycyclic aromatic hydrocarbons in Recent lake sediments-I. Compounds having anthropogenic origins. Geochim. Cosmochim. Acta 44:403-413.
5. Christian JR, Anderson TR. 2002. Modeling DOM biogeochemistry, p 717-755. In Hansell DA, Carlson CA (ed), Biogeochemistry of marine dissolved organic matter. Academic Press, San Diego, CA.
6. Crawford DL, Pometto AL, Crawford RL. 1983. Streptomyces viridosporus: isolation and characterization of a new polymeric lignin degradation intermediate. Appl. Environ. Microbiol. 45:898-904.
7. Alvarez PJJ, Vogel TM. 1991. Substrate interactions of benzene, toluene, and para-xylene during microbial degradation by pure cultures and mixed culture aquifer slurries. Appl. Environ. Microbiol. 57:2981-2985.
8. Kirk TK, Farrell RL. 1987. Enzymatic "combustion": the microbial degradation of lignin. Annu. Rev. Microbiol. 41:465-505.
9. Fuchs G, Boll M, Heider J. 2011. Microbial degradation of aromatic compounds-from one strategy to four. Nat. Rev. Microbiol. 9:803-816.
10. Harwood CS, Parales RE. 1996. The beta-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50:553-590.
11. Stanier RY, Ornston LN. 1973. The beta-ketoadipate pathway. Adv. Microb. Physiol. 9:89-151.
12. Rather LJ, Knapp B, Haehnel W, Fuchs G. 2010. Coenzyme A-dependent aerobic metabolism of benzoate via epoxide formation. J. Biol. Chem. 285:20615-20624.
13. Romero-Steiner S, Parales RE, Harwood CS, Houghton JE. 1994. Characterization of the pcaR regulatory gene from Pseudomonas putida, which is required for the complete degradation of p-hydroxybenzoate. J. Bacteriol. 176:5771-5779.
14. Wheelis ML, Ornston LN. 1972. Genetic control of enzyme induction in the β-ketoadipate pathway of Pseudomonas putida: deletion mapping of cat mutations. J. Bacteriol. 109:790-795.
15. 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.
16. Dal S, Steiner I, Gerischer U. 2002. Multiple operons connected with catabolism of aromatic compounds in Acinetobacter sp. strain ADP1 are under carbon catabolite repression. J. Mol. Microbiol. Biotechnol. 4:389-404.
17. Cánovas JL, Stanier RY. 1967. Regulation of the enzymes of the betaketoadipate pathway in Moraxella calcoacetica. I. General aspects. Eur. J. Biochem. 1:289-300.
18. Brzostowicz PC, Reams AB, Clark TJ, Neidle EL. 2003. Transcriptional cross-regulation of the catechol and protocatechuate branches of the betaketoadipate pathway contributes to carbon source-dependent expression of the Acinetobacter sp. strain ADP1 pobA gene. Appl. Environ. Microbiol. 69:1598-1606.
19. Donoso RA, Pérez-Pantoja D, González B. 2011. 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. 13:1590-1600.
20. Gaines GL, Smith L, Neidle EL. 1996. Novel nuclear magnetic resonance spectroscopy methods demonstrate preferential carbon source utilization by Acinetobacter calcoaceticus. J. Bacteriol. 178:6833-6841.
21. Ornston LN, Stanier RY. 1966. Conversion of catechol and protocatechuate to beta-ketoadipate by Pseudomonas putida. I. Biochemistry. J. Biol. Chem. 241:3776-3786.
22. Siehler SY, Dal S, Fischer R, Patz P, Gerischer U. 2007. Multiple-level regulation of genes for protocatechuate degradation in Acinetobacter baylyi includes cross-regulation. Appl. Environ. Microbiol. 73:232-242.
23. Bleichrodt FS, Fischer R, Gerischer UC. 2010. The beta-ketoadipate pathway of Acinetobacter baylyi undergoes carbon catabolite repression, cross-regulation and vertical regulation, and is affected by Crc. Microbiology 156:1313-1322.
24. del Giorgio PA, Davis J. 2003. Patterns in dissolved organic matter lability and consumption across aquatic ecosystems, p 399-424. In Findlay SEG, Sinsabaugh RL (ed), Aquatic ecosystems: interactivity of dissolved organic matter. Academic Press, San Diego, CA.
25. McCarthy M, Hedges J, Benner R. 1996. Major biochemical composition of dissolved high molecular weight organic matter in seawater. Mar. Chem. 55:281-297.
26. Suzuki MT, Preston CM, Chavez FP, DeLong EF. 2001. Quantitative mapping of bacterioplankton populations in seawater: field tests across an upwelling plume in Monterey Bay. Aquat. Microb. Ecol. 24:117-127.
27. Selje N, Simon M, Brinkhoff T. 2004. A newly discovered Roseobacter cluster in temperate and polar oceans. Nature 427:445-448.
28. Moran MA, Belas R, Schell MA, González JM, Sun F, Sun S, Binder BJ, Edmonds J, Ye W, Orcutt B, Howard EC, Meile C, Palefsky W, Goesmann A, Ren Q, Paulsen I, Ulrich LE, Thompson LS, Saunders E, Buchan A. 2007. Ecological genomics of marine roseobacters. Appl. Environ. Microbiol. 73:4559-4569.
29. Mou X, Sun S, Edwards RA, Hodson RE, Moran MA. 2008. Bacterial carbon processing by generalist species in the coastal ocean. Nature 451: 708-711.
30. Newton RJ, Griffin LE, Bowles KM, Meile C, Gifford S, Givens CE, Howard EC, King E, Oakley CA, Reisch CR, Rinta-Kanto JM, Sharma S, Sun SL, Varaljay V, Vila-Costa M, Westrich JR, Moran MA. 2010. Genome characteristics of a generalist marine bacterial lineage. ISME J. 4:784-798.
31. Rocker D, Brinkhoff T, Grüner N, Dogs M, Simon M. 2012. Composition of humic acid-degrading estuarine and marine bacterial communities. FEMS Microbiol. Ecol. 80:45-63.
32. González JM, Mayer F, Moran MA, Hodson RE, Whitman WB. 1997. Sagittula stellata gen. nov., sp. nov., a lignin-transforming bacterium from a coastal environment. Int. J. Syst. Bacteriol. 47:773-780.
33. Jamieson WD, Pehl MJ, Gregory GA, Orwin PM. 2009. Coordinated surface activities in Variovorax paradoxus EPS. BMC Microbiol. 9:124. doi:10.1186/1471-2180-9-124.
34. Cude WN, Mooney J, Tavanaei AA, Hadden MK, Frank AM, Gulvik CA, May AL, Buchan A. 2012. Production of the antimicrobial secondary metabolite indigoidine contributes to competitive surface colonization in the marine roseobacter Phaeobacter sp. strain Y4I. Appl. Environ. Microbiol. 78:4771-4780.
35. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J. 2007. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8:R19. doi:10.1186/gb-2007-8-2-r19.
36. Stanier RY, Ingraham JL. 1954. Protocatechuic acid oxidase. J. Biol. Chem. 210:799-808.
37. 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.
38. Buchan A, Neidle EL, Moran MA. 2004. Diverse organization of genes of the beta-ketoadipate pathway in members of the marine Roseobacter lineage. Appl. Environ. Microbiol. 70:1658-1668.
39. Buchan A, Collier LS, Neidle EL, Moran MA. 2000. Key aromatic-ringcleaving enzyme, protocatechuate 3,4-dioxygenase, in the ecologically important marine Roseobacter lineage. Appl. Environ. Microbiol. 66:4662-4672.
40. DiMarco AA, Averhoff B, Ornston LN. 1993. Identification of the transcriptional activator pobR and characterization of its role in the expression of pobA, the structural gene for p-hydroxybenzoate hydroxylase in Acinetobacter calcoaceticus. J. Bacteriol. 175:4499-4506.
41. DiMarco AA, Ornston LN. 1994. Regulation of p-hydroxybenzoate hydroxylase synthesis by PobR bound to an operator in Acinetobacter calcoaceticus. J. Bacteriol. 176:4277-4284.
42. Quinn JA, McKay DB, Entsch B. 2001. Analysis of the pobA and pobR genes controlling expression of p-hydroxybenzoate hydroxylase in Azotobacter chroococcum. Gene 264:77-85.
43. Harder W, Dijkhuizen L. 1982. Strategies of mixed substrate utilization in microorganisms. Philos. Trans. R. Soc. Lond. B Biol. Sci. 297:459-480.
44. Zylstra GJ, Olsen RH, Ballou DP. 1989. Cloning, expression, and regulation of the Pseudomonas cepacia protocatechuate 3,4-dioxygenase genes. J. Bacteriol. 171:5907-5914.
45. Hugouvieux-Cotte-Pattat N, Köhler T, Rekik M, Harayama S. 1990. Growth-phase-dependent expression of the Pseudomonas putida TOL plasmid pWW0 catabolic genes. J. Bacteriol. 172:6651-6660.
46. Kamogawa A, Kurahash K. 1967. Inhibitory effect of glucose on the growth of a mutant strain of Escherichia coli defective in glucose transport system. J. Biochem. 61:220-230.
47. Nichols NN, Harwood CS. 1995. Repression of 4-hydroxybenzoate transport and degradation by benzoate: a new layer of regulatory control in the Pseudomonas putida beta-ketoadipate pathway. J. Bacteriol. 177:7033-7040.
48. Ampé F, Lindley ND. 1995. Acetate utilization is inhibited by benzoate in Alcaligenes eutrophus: evidence for transcriptional control of the expression of acoE coding for acetyl coenzyme A synthetase. J. Bacteriol. 177: 5826-5833.
49. Fujihara H, Yoshida H, Matsunaga T, Goto M, Furukawa K. 2006. Cross-regulation of biphenyl-and salicylate-catabolic genes by two regulatory systems in Pseudomonas pseudoalcaligenes KF707. J. Bacteriol. 188: 4690-4697.
50. Zwaig N, Lin ECC. 1966. Feedback inhibition of glycerol kinase, a catabolic enzyme in Escherichia coli. Science 153:755-757.
51. Heinaru E, Viggor S, Vedler E, Truu J, Merimaa M, Heinaru A. 2001. Reversible accumulation of p-hydroxybenzoate and catechol determines the sequential decomposition of phenolic compounds in mixed substrate cultivations in pseudomonads. FEMS Microbiol. Ecol. 37:79-89.
52. van der Kooij D, Oranje JP, Hijnen WAM. 1982. Growth of Pseudomonas aeruginosa in tap water in relation to utilization of substrates at concentrations of a few micrograms per liter. Appl. Environ. Microbiol. 44: 1086-1095.
53. Poindexter JS. 1981. Oligotrophy. Fast and famine existence. Adv. Microb. Ecol. 5:63-89.
54. Egli T. 2010. How to live at very low substrate concentration. Water Res. 44:4826-4837.
55. Moran MA, Hodson RE. 1990. Contributions of degrading Spartina alterniflora lignocellulose to the dissolved organic carbon pool of a salt marsh. Mar. Ecol. Prog. Ser. 62:161-168.
56. Buchan A, Newell SY, Butler M, Biers EJ, Hollibaugh JT, Moran MA. 2003. Dynamics of bacterial and fungal communities on decaying salt marsh grass. Appl. Environ. Microbiol. 69:6676-6687.
57. Moran MA, Hodson RE. 1994. Dissolved humic substance of vascular plant origin in a coastal marine environment. Limnol. Oceanogr. 39:762-771.
58. Gerischer U, Segura A, Ornston LN. 1998. PcaU, a transcriptional activator of genes for protocatechuate utilization in Acinetobacter. J. Bacteriol. 180:1512-1524.
59. Buchan A, González JM. 2010. Roseobacter, p 1336-1343. In Timmis KN (ed), Handbook of hydrocarbon and lipid microbiology. Springer-Verlag, Berlin, Germany.
60. Wood AP, Kelly DP. 1977. Heterotrophic growth of Thiobacillus A2 on sugars and organic acids. Arch. Microbiol. 113:257-264.
61. Wood AP, Kelly DP. 1982. Kinetics of sugar transport by Thiobacillus A2. Arch. Microbiol. 131:156-159.
62. Wood AP, Kelly DP. 1982. Mechanisms of sugar transport by Thiobacillus A2. Arch. Microbiol. 131:160-164.
63. Harwood CS, Nichols NN, Kim MK, Ditty JL, Parales RE. 1994. Identification of the pcaRKF gene cluster from Pseudomonas putida-involvement in chemotaxis, biodegradation, and transport of 4-hydroxybenzoate. J. Bacteriol. 176:6479-6488.
64. Thayer JR, Wheelis ML. 1976. Characterization of a benzoate permease mutant of Pseudomonas putida. Arch. Microbiol. 110:37-42.
65. Collier LS, Nichols NN, Neidle EL. 1997. benK encodes a hydrophobic permease-like protein involved in benzoate degradation by Acinetobacter sp. strain ADP1. J. Bacteriol. 179:5943-5946.