Microbial Ecology

, Volume 73, Issue 2, pp 353–367 | Cite as

Microbial Degradation of Polyhydroxyalkanoates with Different Chemical Compositions and Their Biodegradability

  • Tatiana G. Volova
  • Svetlana V. Prudnikova
  • Olga N. Vinogradova
  • Darya A. Syrvacheva
  • Ekaterina I. Shishatskaya
Environmental Microbiology

Abstract

The study addresses degradation of polyhydroxyalkanoates (PHA) with different chemical compositions—the polymer of 3-hydroxybutyric acid [P(3HB)] and copolymers of P(3HB) with 3-hydroxyvalerate [P(3HB/3HV)], 4-hydroxybutyrate [P(3HB/4HB)], and 3-hydroxyhexanoate [P(3HB/3HHx)] (10–12 mol%)—in the agro-transformed field soil of the temperate zone. Based on their degradation rates at 21 and 28 °C, polymers can be ranked as follows: P(3HB/4HB) > P(3HB/3HHx) > P(3HB/3HV) > P(3HB). The microbial community on the surface of the polymers differs from the microbial community of the soil with PHA specimens in the composition and percentages of species. Thirty-five isolates of bacteria of 16 genera were identified as PHA degraders by the clear zone technique, and each of the PHA had both specific and common degraders. P(3HB) was degraded by bacteria of the genera Mitsuaria, Chitinophaga, and Acidovorax, which were not among the degraders of the three other PHA types. Roseateles depolymerans, Streptomyces gardneri, and Cupriavidus sp. were specific degraders of P(3HB/4HB). Roseomonas massiliae and Delftia acidovorans degraded P(3HB/3HV), and Pseudoxanthomonas sp., Pseudomonas fluorescens, Ensifer adhaerens, and Bacillus pumilus were specific P(3HB/3HHx) degraders. All four PHA types were degraded by Streptomyces.

Keywords

Degradable polyhydroxyalkanoates PHA Soil PHA-degrading microorganisms 

References

  1. 1.
    Arcos-Hernandez MV, Laycock B, Pratt S, Donose BC, Nikolić MA, Luckman P, Werker A, Lant PA (2012) Biodegradation in a soil environment of activated sludge derived polyhydroxyalkanoate (PHBV). Polym Degrad Stab 97:2301–2312. doi:10.1016/j.polymdegradstab.2012.07.035 CrossRefGoogle Scholar
  2. 2.
    Bateman GL, Murray G (2001) Seasonal variations in populations of Fusarium species in wheat-field soil. Appl Soil Ecol 18:117–128. doi:10.1016/S0929-1393(01)00158-5 CrossRefGoogle Scholar
  3. 3.
    Boyandin AN, Prudnikova SV, Karpov VA, Ivonin VN, Đỗ NL, Nguyễn TH, Lê TMH, Filichev NL, Levin AL, Filipenko ML, Volova TG, Gitelson II (2013) Microbial degradation of polyhydroxyalkanoates in tropical soils. Int Biodeterior Biodegrad 83:77–84. doi:10.1016/j.ibiod.2013.04.014 CrossRefGoogle Scholar
  4. 4.
    Boyandin AN, Rudnev VP, Ivonin VN, Prudnikova SV, Korobikhina KI, Filipenko ML, Volova TG, Sinskey AJ (2012) Biodegradation of polyhydroxyalkanoate films in natural environments. Macromol Symp 320:38–42. doi:10.1002/masy.201251004 CrossRefGoogle Scholar
  5. 5.
    Brandl H, Püchner P (1991) Biodegradation of plastic bottles made from ‘Biopol’ in an aquatic ecosystem under in situ conditions. Biodegradation 2:237–243. doi:10.1007/BF00114555 CrossRefGoogle Scholar
  6. 6.
    Briese BH, Jendrossek D, Schlegel HG (1994) Degradation of poly (3‐hydroxybutyrate‐co‐3‐hydroxyvalerate) by aerobic sewage sludge. FEMS Microbiol Lett 117:107–111. doi:10.1111/j.1574-6968.1994.tb06750.x CrossRefPubMedGoogle Scholar
  7. 7.
    Brunel DG, Pachekoski WM, Dalmolin C, Agnelli JAM (2014) Natural additives for poly (hydroxybutyrate-co-hydroxyvalerate)-PHBV: effect on mechanical properties and biodegradation. Mater Res 17:1145–1156. doi:10.1590/1516-1439.235613 CrossRefGoogle Scholar
  8. 8.
    Bugnicourt E, Cinelli P, Lazzeri A, Alvarez V (2014) Polyhydroxyalkanoate (PHA): review of synthesis, characteristics, processing and potential applications in packaging. Express Polym Lett 8:791–808. doi:10.3144/expresspolymlett.2014.82 CrossRefGoogle Scholar
  9. 9.
    Calabia BP, Tokiwa Y (2006) A novel PHB depolymerase from a thermophilic Streptomyces sp. Biotechnol Lett 28:383–388. doi:10.1007/s10529-005-6063-5 CrossRefPubMedGoogle Scholar
  10. 10.
    Choi MK, Kim KD, Ahn KM, Shin DH, Hwang JH, Seong CN, Ka JO (2009) Genetic and phenotypic diversity of parathion-degrading bacteria isolated from rice paddy soils. J Microbiol Biotechnol 19:1679–1687. doi:10.4014/jmb.0905.05057 CrossRefPubMedGoogle Scholar
  11. 11.
    Chowdhury AA (1963) Poly-β-hydroxybuttersäure abbauende bakterien und exoenzym. Arch Microbiol 47:167–200. doi:10.1007/BF00422523 Google Scholar
  12. 12.
    Delafield FP, Doudoroff M, Palleroni NJ, Lusty CJ, Contopoulos R (1965) Decomposition of poly-β-hydroxybutyrate by pseudomonads. J Bacteriol 90:1455–1466, PMCID: PMC315835PubMedPubMedCentralGoogle Scholar
  13. 13.
    Deroiné M, César G, Le Duigou A, Davies P, Bruzaud S (2015) Natural degradation and biodegradation of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) in liquid and solid marine environments. J Polym Environ 23:493–505. doi:10.1007/s10924-015-0736-5 CrossRefGoogle Scholar
  14. 14.
    Doi Y, Kanesawa Y, Tanahashi N, Kumagai Y (1992) Biodegradation of microbial polyesters in the marine environment. Polym Degrad Stab 36:173–177. doi:10.1016/0141-3910(92)90154-W CrossRefGoogle Scholar
  15. 15.
    Elbanna K, Lütke-Eversloh T, Jendrossek D, Luftmann H, Steinbüchel A (2004) Studies on the biodegradability of polythioester copolymers and homopolymers by polyhydroxyalkanoate (PHA)-degrading bacteria and PHA depolymerases. Arch Microbiol 182:212–225. doi:10.1007/s00203-004-0715-z CrossRefPubMedGoogle Scholar
  16. 16.
    Futamata H, Nagano Y, Watanabe K, Hiraishi A (2005) Unique kinetic properties of phenol-degrading Variovorax strains responsible for efficient trichloroethylene degradation in a chemostat enrichment culture. Appl Environ Microbiol 71:904–911. doi:10.1128/AEM.71.2.904-911.2005 CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Garrity GM, Brenner DJ, Krieg NR, Staley JR (eds) (2005) Bergey’s Manual of Systematic Bacteriology, vol 2. The Proteobacteria. 2 ed. Springer, New YorkGoogle Scholar
  18. 18.
    Holt JG, Krieg NR, Sneath PHA, Staley JT, Williams ST (eds) (1994) Bergey’s Manual of Determinative Bacteriology, 9th edition. Williams & Wilkins, BaltimoreGoogle Scholar
  19. 19.
    Imam SH, Gordon SH, Shogren RL, Tosteson TR, Govind NS, Greene RV (1999) Degradation of starch-poly (β-hydroxybutyrate-co-β-hydroxyvalerate) bioplastic in tropical coastal waters. Appl Environ Microbiol 65:431–437, PMCID: PMC91043 PubMedPubMedCentralGoogle Scholar
  20. 20.
    Jendrossek D, Handrick R (2002) Microbial degradation of polyhydroxyalkanoates. Ann Rev Microbiol 56:403–432. doi:10.1146/annurev.micro.56.012302.160838 CrossRefGoogle Scholar
  21. 21.
    Jiang Y, Ye J, Wu H, Zhang H (2004) Cloning and expression of the polyhydroxyalkanote depolymerase gene from Pseudomonas putida, and characterization of the gene product. Biotechnol Lett 26:1585–1588. doi:10.1023/B:BILE.0000045657.93818.18 CrossRefPubMedGoogle Scholar
  22. 22.
    Kim DY, Kim HC, Kim SY, Rhee YH (2005) Molecular characterization of extracellular medium-chain-length poly (3-hydroxyalkanoate) depolymerase genes from Pseudomonas alcaligenes strains. J Microbiol 43:285–294Google Scholar
  23. 23.
    Kozlovsky AG, Zhelifonova VP, Vinokourova NG, Antipova TV, Ivanushkina NE (1999) The study of biodegradation of poly-β-hydroxybutyrate by microscopic fungi. Microbiology 68:340–346 (In Russian)Google Scholar
  24. 24.
    Kunioka M, Kawaguchi Y, Doi Y (1989) Production of biodegradable copolyesters of 3-hydroxybutyrate and 4-hydroxybutyrate by Alcaligenes eutrophus. Appl Microbiol Biotechnol 30:569–573. doi:10.1007/BF00255361 CrossRefGoogle Scholar
  25. 25.
    Kusaka S, Iwata T, Do Y (1999) Properties and biodegradability of ultra-high-molecular-weight poly [(R)-3-hydroxybutyrate] produced by a recombinant Escherichia coli. Int J Biol Macromol 25:87–94. doi:10.1016/S0141-8130(99)00019-7 CrossRefPubMedGoogle Scholar
  26. 26.
    Lee KM, Gimore DF, Huss MJ (2005) Fungal degradation of the bioplastic PHB (poly-3-hydroxy-butyric acid). J Polym Environ 13:213–219. doi:10.1007/s10924-005-4756-4 CrossRefGoogle Scholar
  27. 27.
    Mabrouk MM, Sabry SA (2001) Degradation of poly (3-hydroxybutyrate) and its copolymer poly (3-hydroxybutyrate-co-3-hydroxyvalerate) by a marine Streptomyces sp. SNG9. Microbiol Res 156:323–335. doi:10.1078/0944-5013-00115 CrossRefPubMedGoogle Scholar
  28. 28.
    Madbouly SA, Schrader JA, Srinivasan G, Liu K, McCabe KG, Grewell D, Graves WR, Kessler MR (2014) Biodegradation behavior of bacterial-based polyhydroxyalkanoate (PHA) and DDGS composites. Green Chem 16:1911–1920. doi:10.1039/C3GC41503A CrossRefGoogle Scholar
  29. 29.
    Madden LA, Anderson AJ, Asrar J (1998) Synthesis and characterization of poly (3-hydroxybutyrate) and poly (3-hydroxybutyrate-co-3-hydroxyvalerate) polymer mixtures produced in high-density fed-batch cultures of Ralstonia eutropha (Alcaligenes eutrophus). Macromolecules 31:5660–5667. doi:10.1021/ma980606w CrossRefGoogle Scholar
  30. 30.
    Masood F, Yasin T, Hameed A (2014) Comparative oxo-biodegradation study of poly-3-hydroxybutyrate-co-3-hydroxyvalerate/polypropylene blend in controlled environments. Int Biodeterior Biodegrad 87:1–8. doi:10.1016/j.ibiod.2013.09.023 CrossRefGoogle Scholar
  31. 31.
    Mergaert J, Anderson C, Wouters A, Swings J (1994) Microbial degradation of poly (3-hydroxybutyrate) and poly (3-hydroxybutyrate-co-3-hydroxyvalerate) in compost. J Environ Polym Degrad 2:177–183. doi:10.1007/BF02067443 CrossRefGoogle Scholar
  32. 32.
    Mergaert J, Webb A, Anderson C, Wouters A, Swings J (1993) Microbial degradation of poly (3-hydroxybutyrate) and poly (3-hydroxybutyrate-co-3-hydroxyvalerate) in soils. Appl Environ Microbiol 59:3233–3238PubMedPubMedCentralGoogle Scholar
  33. 33.
    Mergaert J, Wouters A, Swings J, Anderson C (1995) In situ biodegradation of poly (3-hydroxybutyrate) and poly (3-hydroxybutyrate-co-3-hydroxyvalerate) in natural waters. Can J Microbiol 41:154–159. doi:10.1139/m95-182 CrossRefPubMedGoogle Scholar
  34. 34.
    Morse MC, Liao Q, Criddle CS, Frank CW (2011) Anaerobic biodegradation of the microbial copolymer poly (3-hydroxybutyrate-co-3-hydroxyhexanoate): effects of comonomer content, processing history, and semi-crystalline morphology. Polymer 52:547–556. doi:10.1016/j.polymer.2010.11.024 CrossRefGoogle Scholar
  35. 35.
    Netrusov AI (2005) Practical course in microbiology. Akademiya, Moscow (In Russian)Google Scholar
  36. 36.
    Oda Y, Asari H, Urakami T, Tonomura K (1995) Microbial degradation of poly (3-hydroxybutyrate) and polycaprolactone by filamentous fungi. J Ferment Bioeng 80:265–269. doi:10.1016/0922-338X(95)90827-M CrossRefGoogle Scholar
  37. 37.
    Quinteros R, Goodwin S, Lenz RW, Park WH (1999) Extracellular degradation of medium chain length poly (β-hydroxyalkanoates) by Comamonas sp. Int J Biol Macromol 25:135–143. doi:10.1016/S0141-8130(99)00027-6 CrossRefPubMedGoogle Scholar
  38. 38.
    Rehman RA, Rao AQ, Ahmed Z, Gul A (2015) Selection of potent bacterial strain for over-production of PHB by using low cost carbon source for eco-friendly bioplastics. Adv Life Sci 3:29–35Google Scholar
  39. 39.
    Rhee YH, Kim YH, Shin KS (2006) Characterization of an extracellular poly (3-hydroxyoctanoate) depolymerase from the marine isolate Pseudomonas luteola M13-4. Enzym Microb Technol 38:529–535. doi:10.1016/j.enzmictec.2005.07.006 CrossRefGoogle Scholar
  40. 40.
    Rodriguez-Contreras A, Calafell-Monfort M, Marqués-Calvo MS (2012) Enzymatic degradation of poly (3-hydroxybutyrate-co-4-hydroxybutyrate) by commercial lipases. Polym Degrad Stab 97:597–604. doi:10.1016/j.polymdegradstab.2012.01.007 CrossRefGoogle Scholar
  41. 41.
    Romen F, Reinhardt S, Jendrossek D (2004) Thermotolerant poly (3-hydroxybutyrate)-degrading bacteria from hot compost and characterization of the PHB depolymerase of Schlegelella sp. KB1a. Arch Microbiol 182:157–164. doi:10.1007/s00203-004-0684-2 CrossRefPubMedGoogle Scholar
  42. 42.
    Ruka DR, Sangwan P, Garvey CJ, Simon GP, Dean KM (2015) Biodegradability of poly-3-hydroxybutyrate/bacterial cellulose composites under aerobic conditions, measured via evolution of carbon dioxide and spectroscopic and diffraction methods. Environ Sci Technol 49:9979–9986. doi:10.1021/es5044485 CrossRefPubMedGoogle Scholar
  43. 43.
    Salim YS, Sharon A, Vigneswari S, Ibrahim MM, Amirul AA (2012) Environmental degradation of microbial polyhydroxyalkanoates and oil palm-based composites. Appl Biochem Biotechnol 167:314–326. doi:10.1007/s12010-012-9688-6 CrossRefPubMedGoogle Scholar
  44. 44.
    Shah AA, Hasan F, Hameed A, Ahmed S (2007) Isolation and characterization of poly (3-hydroxybutyrate-co-3-hydroxyvalerate) degrading bacteria and purification of PHBV depolymerase from newly isolated Bacillus sp. AF3. Int Biodeterior Biodegrad 60:109–115. doi:10.1016/j.ibiod.2007.01.004 CrossRefGoogle Scholar
  45. 45.
    Sridewi N, Bhubalan K, Sudesh K (2006) Degradation of commercially important polyhydroxyalkanoates in tropical mangrove ecosystem. Polym Degrad Stab 91:2931–2940. doi:10.1016/j.polymdegradstab.2006.08.027 CrossRefGoogle Scholar
  46. 46.
    Sutton D, Fothergill A, Rinaldi M (2001) Guide to pathogenic and opportunistic fungi (Trans. from English). Mir, Moscow (In Russian)Google Scholar
  47. 47.
    Suyama T, Tokiwa Y, Ouichanpagdee P, Kanagawa T, Kamagata Y (1998) Phylogenetic affiliation of soil bacteria that degrade aliphatic polyesters available commercially as biodegradable plastics. Appl Environ Microbiol 64:5008–5011, PMCID: PMC90957 PubMedPubMedCentralGoogle Scholar
  48. 48.
    Takeda M, Koizumi JI, Yabe K, Adachi K (1998) Thermostable poly (3-hydroxybutyrate) depolymerase of a thermophilic strain of Leptothrix sp. isolated from a hot spring. J Ferment Bioeng 85:375–380. doi:10.1016/S0922-338X(98)80080-9 CrossRefGoogle Scholar
  49. 49.
    Tamura K, Stecher G., Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol mst197. doi:10.1093/molbev/mst197
  50. 50.
    Tani A, Akita M, Murase H, Kimbara K (2011) Culturable bacteria in hydroponic cultures of moss Racomitrium japonicum and their potential as biofertilizers for moss production. J Biosci Bioeng 112:32–39. doi:10.1016/j.jbiosc.2011.03.012 CrossRefPubMedGoogle Scholar
  51. 51.
    Volova TG, Belyaeva OG, Plotnikov VF, Puzyr AP (1998) Studies of biodegradation of microbial polyhydroxyalkanoates. Appl Biochem Microbiol 34:488–492Google Scholar
  52. 52.
    Volova TG, Boyandin AN, Vasil’ev AD, Karpov VA, Kozhevnikov IV, Prudnikova SV, Rudnev VP, Büi BX, Vũ VD, Gitel’Zon II (2011) Biodegradation of polyhydroxyalkanoates (PHAs) in the South China Sea and identification of PHA-degrading bacteria. Microbiology 80:252–260CrossRefGoogle Scholar
  53. 53.
    Volova TG, Boyandin AN, Vasiliev AD, Karpov VA, Prudnikova SV, Mishukova OV, Boyarskikh UA, Filipenko ML, Rudnev VP, Büi BX, Vũ VD, Gitel’Zon II (2010) Biodegradation of polyhydroxyalkanoates (PHAs) in tropical coastal waters and identification of PHA-degrading bacteria. Polym Degrad Stab 95:2350–2359. doi:10.1016/j.polymdegradstab.2010.08.023 CrossRefGoogle Scholar
  54. 54.
    Volova TG, Gladyshev MI, Trusova MY, Zhila NO (2007) Degradation of polyhydroxyalkanoates in eutrophic reservoir. Polym Degrad Stab 92:580–586. doi:10.1016/j.polymdegradstab.2007.01.011 CrossRefGoogle Scholar
  55. 55.
    Volova TG, Kiselev EG, Shishatskaya EI, Zhila NO, Boyandin AN, Syrvacheva DA, Vinogradova ON, Kalacheva GS, Vasiliev AD, Peterson IV (2013) Cell growth and accumulation of polyhydroxyalkanoates from CO2 and H2 of a hydrogen-oxidizing bacterium, Cupriavidus eutrophus B-10646. Bioresour Technol 146:215–222. doi:10.1016/j.biortech.2013.07.070 CrossRefPubMedGoogle Scholar
  56. 56.
    Volova TG, Kiselev EG, Vinogradova ON, Nikolaeva ED, Chistyakov AA, Sukovatyi AG, Shishatskaya EI (2014) A glucose-utilizing strain, Cupriavidus eutrophus B-10646: growth kinetics, characterization and synthesis of multicomponent PHAs. PLoS One 9:1–15. doi:10.1371/journal.pone.0087551 CrossRefGoogle Scholar
  57. 57.
    Vos PD, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer KH, Whitman W (eds) (2009) Bergey’s Manual of Systematic Bacteriology, vol 3. The Firmicutes. 2 ed. Springer, New YorkGoogle Scholar
  58. 58.
    Wang YW, Mo W, Yao H, Wu Q, Chen J, Chen GQ (2004) Biodegradation studies of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). Polym Degrad Stab 85:815–821. doi:10.1016/j.polymdegradstab.2004.02.010 CrossRefGoogle Scholar
  59. 59.
    Watanabe T (2002) Pictorial atlas of soil and seed fungi: morphologies of cultured fungi and key to species, 2nd edn. CRC Press, Boca RatonGoogle Scholar
  60. 60.
    Wen X, Lu X (2012) Microbial degradation of poly (3-hydroxybutyrate-co-4-hydroxybutyrate) in soil. J Polym Environ 20:381–387. doi:10.1007/s10924-011-0387-0 CrossRefGoogle Scholar
  61. 61.
    Weng YX, Wang L, Zhang M, Wang XL, Wang YZ (2013) Biodegradation behavior of P (3HB, 4HB)/PLA blends in real soil environments. Polym Test 32:60–70. doi:10.1016/j.polymertesting.2012.09.014 CrossRefGoogle Scholar
  62. 62.
    Weng YX, Wang XL, Wang YZ (2011) Biodegradation behavior of PHAs with different chemical structures under controlled composting conditions. Polym Test 30:372–380. doi:10.1016/j.polymertesting.2011.02.001 CrossRefGoogle Scholar
  63. 63.
    Zhila N, Prudnikova S, Zadereev E, Rogozin D (2012) Degradation of polyhydroxyalkanoates in brackish Lake Shira. J Sib Fed Univ Ser Biol 5:210–215 (In Russian)Google Scholar
  64. 64.
    Zvyagintsev DG (1991) Methods of soil microbiology and biochemistry. The Moscow State University Press, Moscow (In Russian)Google Scholar
  65. 65.
    Zvyagintsev DG, Bab’eva IP, Zenova GM (2005) Soil biology. The Moscow State University Press, Moscow (In Russian)Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Tatiana G. Volova
    • 1
  • Svetlana V. Prudnikova
    • 1
  • Olga N. Vinogradova
    • 1
  • Darya A. Syrvacheva
    • 1
  • Ekaterina I. Shishatskaya
    • 1
  1. 1.Institute of Biophysics of Siberian Branch of Russian Academy of SciencesKrasnoyarskRussia

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