Advertisement

Applied Microbiology and Biotechnology

, Volume 102, Issue 5, pp 2117–2127 | Cite as

A novel biological recovery approach for PHA employing selective digestion of bacterial biomass in animals

  • Su Yean Ong
  • Idris Zainab-L
  • Somarajan Pyary
  • Kumar Sudesh
Mini-Review
  • 438 Downloads

Abstract

Polyhydroxyalkanoate (PHA) is a family of microbial polyesters that is completely biodegradable and possesses the mechanical and thermal properties of some commonly used petrochemical-based plastics. Therefore, PHA is attractive as a biodegradable thermoplastic. It has always been a challenge to commercialize PHA due to the high cost involved in the biosynthesis of PHA via bacterial fermentation and the subsequent purification of the synthesized PHA from bacterial cells. Innovative enterprise by researchers from various disciplines over several decades successfully reduced the cost of PHA production through the efficient use of cheap and renewable feedstock, precisely controlled fermentation process, and customized bacterial strains. Despite the fact that PHA yields have been improved tremendously, the recovery and purification processes of PHA from bacterial cells remain exhaustive and require large amounts of water and high energy input besides some chemicals. In addition, the residual cell biomass ends up as waste that needs to be treated. We have found that some animals can readily feed on the dried bacterial cells that contain PHA granules. The digestive system of the animals is able to assimilate the bacterial cells but not the PHA granules which are excreted in the form of fecal pellets, thus resulting in partial recovery and purification of PHA. In this mini-review, we will discuss this new concept of biological recovery, the selection of the animal model for biological recovery, and the properties and possible applications of the biologically recovered PHA.

Keywords

Polyhydroxyalkanoate Biological recovery Mealworms Selective digestion Small animals 

Notes

Acknowledgements

The authors would like to acknowledge the funding by Exploratory Research Grant Scheme (203/PBIOLOGI/6730049), and support and research facilities provided by Universiti Sains Malaysia and RIKEN, Japan. SY Ong and I Zainab-L wish to acknowledge the financial support provided by MyBrain15 scholarship from the Ministry of Higher Education and Malaysian International Scholarship, respectively. Pyary would like to thank USM Fellowship and Short-Term IPA Programme at Bioplastic Research Group, RIKEN, Japan, for the financial support. We would like to thank Dr. Manoj Lakshmanan from Universiti Sains Malaysia for the language editing.

Funding information

This research was supported by Exploratory Research Grant Scheme (203/PBIOLOGI/6730049).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

This article does not contain any studies with human participants performed by any of the authors.

References

  1. Anderson AJ, Dawes EA (1990) Occurrence, metabolism, metabolic role, and industrial uses of bacterial polyhydroxyalkanoates. Microbiol Rev 54(4):450–472PubMedPubMedCentralGoogle Scholar
  2. Association of American Plant Food Control Officials (AAPFCO) (1995) Official Publication No. 48. Published by Association of American Plant Food Control Officials, Inc., West LafayetteGoogle Scholar
  3. Barroso FG, de Haro C, Sánchez-Muros M-J, Venegas E, Martínez-Sánchez A, Pérez-Bañón C (2014) The potential of various insect species for use as food for fish. Aquaculture 422:193–201CrossRefGoogle Scholar
  4. Boon N, Defoirdt T, De Windt W, Van De Wiele T, Verstraete W (2013) Universiteit Gent, assignee. Hydroxybutyrate and poly-hydroxybutyrate as components of animal feed or feed additives. United States patent US 8,603,518. 2013 Dec 10Google Scholar
  5. Budde CF, Riedel SL, Willis LB, Rha C, Sinskey AJ (2011) Production of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) from plant oil by engineered Ralstonia eutropha strains. Appl Environ Microbiol 77(9):2847–2854.  https://doi.org/10.1128/AEM.02429-10 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Calloway DH, Kumar AM (1969) Protein quality of the bacterium Hydrogenomonas eutropha. Appl Microbiol 17(1):176–178PubMedPubMedCentralGoogle Scholar
  7. Chen G, Zhang G, Park S, Lee S (2011) Industrial scale production of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate). App Microbiol Biotechnol 57(1–2):50–55Google Scholar
  8. Chien S, Prochnow L, Cantarella H (2009) Recent developments of fertilizer production and use to improve nutrient efficiency and minimize environmental impacts. Adv Agron 102:267–322CrossRefGoogle Scholar
  9. Choi MH, Park YH (2003) Production of yeast biomass using waste Chinese cabbage. Biomass Bioenergy 25(2):221–226.  https://doi.org/10.1016/S0961-9534(02)00194-0 CrossRefGoogle Scholar
  10. Costa-Neto EM (2005) Entomotherapy, or the medicinal use of insects. J Ethnobiol 25(1):93–114.Google Scholar
  11. Davis GR (1975) Essential dietary amino acids for growth of larvae of the yellow mealworm, Tenebrio molitor L. J Nutr 105(8):1071–1075.  https://doi.org/10.1093/jn/105.8.1071 CrossRefPubMedGoogle Scholar
  12. Doi Y (1990) Microbial polyesters. VCH, New YorkGoogle Scholar
  13. Dossey AT, Morales-Ramos JA, Rojas MG (2016) Insects as sustainable food ingredients: production, processing and food applications. Academic Press, CambridgeGoogle Scholar
  14. Edozien JC, Udo UU, Young VR, Scrimshaw NS (1970) Effects of high levels of yeast feeding on uric acid metabolism of young men. Nature 228(5267):180.  https://doi.org/10.1038/228180a0 CrossRefPubMedGoogle Scholar
  15. Elpidina EN, Goptar IA (2007) Digestive peptidases in Tenebrio molitor and possibility of use to treat celiac disease. Entomol Res 37(3):139–147.  https://doi.org/10.1111/j.1748-5967.2007.00103.x CrossRefGoogle Scholar
  16. Engel P, Moran NA (2013) The gut microbiota of insects–diversity in structure and function. FEMS Microbiol Rev 37(5):699–735.  https://doi.org/10.1111/1574-6976.12025 CrossRefPubMedGoogle Scholar
  17. Ferreira C, Bellinello GL, Ribeiro AF, Terra WR (1990) Digestive enzymes associated with the glycocalyx, microvillar membranes and secretory vesicles from midgut cells of Tenebrio molitor larvae. Insect Biochem 20(8):839–847.  https://doi.org/10.1016/0020-1790(90)90102-Z CrossRefGoogle Scholar
  18. Fraenkel G (1950) The nutrition of the mealworm, Tenebrio molitor L. (Tenebrionidae, Coleoptera). Physiol Zool 23(2):92–108.  https://doi.org/10.1086/physzool.23.2.30152067 CrossRefPubMedGoogle Scholar
  19. Fukui T, Abe H, Doi Y (2002) Engineering of Ralstonia eutropha for production of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) from fructose and solid-state properties of the copolymer. Biomacromolecules 3(3):618–624.  https://doi.org/10.1021/bm0255084 CrossRefPubMedGoogle Scholar
  20. Ghisellini P, Cialani C, Ulgiati S (2016) A review on circular economy: the expected transition to a balanced interplay of environmental and economic systems. J Clean Prod 114:11–32CrossRefGoogle Scholar
  21. Gullan PJ, Cranston PS (2014) The insects: an outline of entomology. John Wiley & Sons, Chapman & Hall, OxfordGoogle Scholar
  22. Husby CE, Niemiera AX, Harris JR, Wright RD (2003) Influence of diurnal temperature on nutrient release patterns of three polymer-coated fertilizers. Hortscience 38:387–389Google Scholar
  23. Iaconisi V, Marono S, Parisi G, Gasco L, Genovese L, Maricchiolo G, Bovera F, Piccolo G (2017) Dietary inclusion of Tenebrio molitor larvae meal: effects on growth performance and final quality treats of blackspot sea bream (Pagellus bogaraveo). Aquaculture 476:49–58.  https://doi.org/10.1016/j.aquaculture.2017.04.007 CrossRefGoogle Scholar
  24. Jacquel N, Lo C-W, Wei Y-H, Wu H-S, Wang SS (2008) Isolation and purification of bacterial poly (3-hydroxyalkanoates). Biochem Eng J 39(1):15–27.  https://doi.org/10.1016/j.bej.2007.11.029 CrossRefGoogle Scholar
  25. Jeon J-M, Brigham CJ, Kim Y-H, Kim H-J, Yi D-H, Kim H, Rha C, Sinskey AJ, Yang Y-H (2014) Biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) [P(HB-co-HHx)] from butyrate using engineered Ralstonia eutropha. Appl Microbiol Biotechnol 98(12):5461–5469.  https://doi.org/10.1007/s00253-014-5617-7 CrossRefPubMedGoogle Scholar
  26. Jiang Y, Marang L, Kleerebezem R, Muyzer G, van Loosdrecht M (2011) Polyhydroxybutyrate production from lactate using a mixed microbial culture. Biotechnol Bioeng 108:2022–2035CrossRefPubMedGoogle Scholar
  27. Jung J, Heo A, Park YW, Kim YJ, Koh H, Park W (2014) Gut microbiota of Tenebrio molitor and their response to environmental change. J Microbiol Biotechnol 24(7):888–897.  https://doi.org/10.4014/jmb.1405.05016 CrossRefPubMedGoogle Scholar
  28. Kinoshita K, Osakada F, Ueda Y, Narasimhan K, Cearley AC, Yee K, Noda I (2006) Kaneka Corp, Procter, Gamble Co, assignee. Method for producing polyhydroxyalkanoate crystal. United States patent US 7,098,298. 2006 Aug 29Google Scholar
  29. Kumar T, Singh M, Purohit H, Kalia V (2009) Potential of Bacillus sp. to produce polyhydroxybutyrate from biowaste. J Appl Microbiol 106(6):2017–2023.  https://doi.org/10.1111/j.1365-2672.2009.04160.x CrossRefPubMedGoogle Scholar
  30. Kunasundari B, Sudesh K (2011) Isolation and recovery of microbial polyhydroxyalkanoates. Express Polym Lett 5(7):620–634.  https://doi.org/10.3144/expresspolymlett.2011.60 CrossRefGoogle Scholar
  31. Kunasundari B, Murugaiyah V, Kaur G, Maurer FH, Sudesh K (2013) Revisiting the single cell protein application of Cupriavidus necator H16 and recovering bioplastic granules simultaneously. PLoS One 8(10):e78528.  https://doi.org/10.1371/journal.pone.0078528 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kunasundari B, Arza CR, Maurer FH, Murugaiyah V, Kaur G, Sudesh K (2017) Biological recovery and properties of poly(3-hydroxybutyrate) from Cupriavidus necator H16. Sep Purif Technol 172:1–6.  https://doi.org/10.1016/j.seppur.2016.07.043 CrossRefGoogle Scholar
  33. Lafferty RM, Heinzle E, inventors; Agroferm AG (1979) Use of cyclic carbonic acid esters as solvents for poly-(β-hydroxybutyric acid). United States patent US 4,140,741. 1979 Feb 20Google Scholar
  34. Lageveen RG, Huisman GW, Preusting H, Ketelaar P, Eggink G, Witholt B (1988) Formation of polyesters by Pseudomonas oleovorans: effect of substrates on formation and composition of poly-(R)-3-hydroxyalkanoates and poly-(R)-3-hydroxyalkenoates. App Environ Microbiol 54:2924–2932Google Scholar
  35. Loo C-Y, Lee W-H, Tsuge T, Doi Y, Sudesh K (2005) Biosynthesis and characterization of poly (3-hydroxybutyrate-co-3-hydroxyhexanoate) from palm oil products in a Wautersia eutropha mutant. Biotechnol Lett 27(18):1405–1410.  https://doi.org/10.1007/s10529-005-0690-8 CrossRefPubMedGoogle Scholar
  36. Ludwig D, Fiore C (1960) Further studies on the relationship between parental age and the life cycle of the mealworm, Tenebrio molitor. Ann Entomol Soc Am 53(5):595–600.  https://doi.org/10.1093/aesa/53.5.595 CrossRefGoogle Scholar
  37. Makkar HP, Tran G, Heuzé V, Ankers P (2014) State-of-the-art on use of insects as animal feed. Anim Feed Sci Technol 197:1–33.  https://doi.org/10.1016/j.anifeedsci.2014.07.008 CrossRefGoogle Scholar
  38. Moita R, Freches A, Lemos P (2014) Crude glycerol as feedstock for polyhydroxyalkanoates production by mixed microbial cultures. Water Res 58:9–20CrossRefPubMedGoogle Scholar
  39. Morales-Ramos J, Rojas M, Shapiro-Ilan D, Tedders W (2010) Developmental plasticity in Tenebrio molitor (Coleoptera: Tenebrionidae): analysis of instar variation in number and development time under different diets. J Entomol Sci 45(2):75–90.  https://doi.org/10.18474/0749-8004-45.2.75 CrossRefGoogle Scholar
  40. Morales-Ramos J, Rojas M, Shapiro-Ilan D, Tedders W (2011) Self-selection of two diet components by Tenebrio molitor (Coleoptera: Tenebrionidae) larvae and its impact on fitness. Environ Entomol 40(5):1285–1294.  https://doi.org/10.1603/EN10239 CrossRefPubMedGoogle Scholar
  41. Murugan P, Han L, Gan CY, Maurer FH, Sudesh K (2016) A new biological recovery approach for PHA using mealworm, Tenebrio molitor. J Biotechnol 239:98–105.  https://doi.org/10.1016/j.jbiotec.2016.10.012 CrossRefPubMedGoogle Scholar
  42. Ng WK, Liew FL, Ang LP, Wong KW (2001) Potential of mealworm (Tenebrio molitor) as an alternative protein source in practical diets for African catfish, Clarias gariepinus. Aquacult Res 32:273–280.  https://doi.org/10.1046/j.1355-557x.2001.00024.x CrossRefGoogle Scholar
  43. Obreza TA, Rouse RE (2006) Long-term response of Hamlin’Orange trees to controlled-release nitrogen fertilizers. Hort Sci 41:423–426Google Scholar
  44. Ong SY, Sudesh K (2016) Effects of polyhydroxyalkanoate degradation on soil microbial community. Polym Degrad Stab 131:9–19.  https://doi.org/10.1016/j.polymdegradstab.2016.06.024 CrossRefGoogle Scholar
  45. Ong SY, Kho HP, Riedel SL, Kim SW, Gan CY, Taylor TD, Sudesh K (2018) An integrative study on biologically recovered polyhydroxyalkanoates (PHAs) and simultaneous assessment of gut microbiome in yellow mealworm. J Biotechnol 265:31–39.  https://doi.org/10.1016/j.jbiotec.2017.10.017 CrossRefPubMedGoogle Scholar
  46. Panini RL, Freitas LEL, Guimarães AM, Rios C, da Silva MFO, Vieira FN, Fracalossi DM, Samuels RI, Prudêncio ES, Silva CP (2017) Potential use of mealworms as an alternative protein source for Pacific white shrimp: digestibility and performance. Aquaculture 473:115–120.  https://doi.org/10.1016/j.aquaculture.2017.02.008 CrossRefGoogle Scholar
  47. Piccolo G, Iaconisi V, Marono S, Gasco L, Loponte R, Nizza S, Bovera F, Parisi G (2017) Effect of Tenebrio molitor larvae meal on growth performance, in vivo nutrients digestibility, somatic and marketable indexes of gilthead sea bream (Sparus aurata). Anim Feed Sci Technol 226:12–20.  https://doi.org/10.1016/j.anifeedsci.2017.02.007 CrossRefGoogle Scholar
  48. Premalatha M, Abbasi T, Abbasi S (2011) Energy-efficient food production to reduce global warming and ecodegradation: the use of edible insects. Renew Sust Energ Rev 15:4357–4360CrossRefGoogle Scholar
  49. Punzo F, Mutchmor J (1980) Effects of temperature, relative humidity and period of exposure on the survival capacity of Tenebrio molitor (Coleoptera: Tenebrionidae). J Kans Entomol Soc:260–270Google Scholar
  50. Ramos-Elorduy J, González EA, Hernández AR, P ino JM (2002) Use of Tenebrio molitor (Coleoptera: Tenebrionidae) to recycle organic wastes and as feed for broiler chickens. J Econ Entomol 95(1):214–220.  https://doi.org/10.1603/0022-0493-95.1.214 CrossRefPubMedGoogle Scholar
  51. Ramsay JA, Berger E, Voyer R, Chavarie C, Ramsay BA (1994) Extraction of poly-3-hydroxybutyrate using chlorinated solvents. Biotechnol Tech 8(8):589–594.  https://doi.org/10.1007/BF00152152 CrossRefGoogle Scholar
  52. Ravindra P (2000) Value-added food: single cell protein. Biotechnol Adv 18:459–479CrossRefPubMedGoogle Scholar
  53. Reis M, Serafim L, Lemos P, Ramos A, Aguiar F, Van Loosdrecht M (2003) Production of polyhydroxyalkanoates by mixed microbial cultures. Bioprocess Biosyst Eng 25(6):377–385.  https://doi.org/10.1007/s00449-003-0322-4 CrossRefPubMedGoogle Scholar
  54. Schlüter O, Rumpold B, Holzhauser T, Roth A, Vogel RF, Quasigroch W, Vogel S, Heinz V, Jäger H, Bandick N (2016) Safety aspects of the production of foods and food ingredients from insects. Mol Nutr Food Res 61(6)Google Scholar
  55. Shaviv A (2001) Advances in controlled-release fertilizers. Adv Agron 71:1–49.  https://doi.org/10.1016/S0065-2113(01)71011-5 CrossRefGoogle Scholar
  56. Shaviv A (2005) Controlled release fertilizers. IFA International Workshop on Enhanced-Efficiency Fertilizers. Frankfurt. International Fertilizer Industry Association Paris, France, pp 28–30Google Scholar
  57. Siemianowska E, Kosewska A, Aljewicz M, Skibniewska KA, Polak-Juszczak L, Jarocki A, Jedras M (2013) Larvae of mealworm (Tenebrio molitor L.) as European novel food. Agri Sci 4:287Google Scholar
  58. Silva L, Taciro M, Ramos MM, Carter J, Pradella J, Gomez J (2004) Poly(3-hydroxybutyrate) [P(3HB)] production by bacteria from xylose, glucose and sugarcane bagasse hydrolysate. J Ind Microbiol Biotechnol 31(6):245–254.  https://doi.org/10.1007/s10295-004-0136-7 CrossRefPubMedGoogle Scholar
  59. Steinbüchel A, Lütke-Eversloh T (2003) Metabolic engineering and pathway construction for biotechnological production of relevant polyhydroxyalkanoates in microorganisms. Biochem Eng J 16(2):81–96.  https://doi.org/10.1016/S1369-703X(03)00036-6 CrossRefGoogle Scholar
  60. Stoops J, Crauwels S, Waud M, Claes J, Lievens B, Van Campenhout L (2016) Microbial community assessment of mealworm larvae (Tenebrio molitor) and grasshoppers (Locusta migratoria migratorioides) sold for human consumption. Food Microbiol 53(Pt B):122–127.  https://doi.org/10.1016/j.fm.2015.09.010 CrossRefPubMedGoogle Scholar
  61. Suman G, Nupur M, Anuradha S, Pradeep B (2015) Single cell protein production: a review. Int J Curr Microbiol Appl Sci 4:251–262Google Scholar
  62. Terra WR, Ferreira C, Bastos F (1985) Phylogenetic considerations of insect digestion: disaccharideses and the spatial organization of digestion in the Tenebrio molitor larvae. Insect Biochem 15:443–449CrossRefGoogle Scholar
  63. Tracey KM (1958) Effects of parental age on the life cycle of the mealworm, Tenebrio molitor Linnaeus. Ann Entomol Soc Am 51(5):429–432.  https://doi.org/10.1093/aesa/51.5.429 CrossRefGoogle Scholar
  64. Trenkel ME (1997) Controlled-release and stabilized fertilizers in agriculture. Intl. Fert. Ind. Assn, ParisGoogle Scholar
  65. Trenkel ME (2010) Slow- and controlled release and stabilized fertilizers: an option for enhancing nutrient use efficiency in agriculture, 2nd edn. Intl. Fert. Ind, AssnGoogle Scholar
  66. Tschinkel WR, Willson CD (1971) Inhibition of pupation due to crowding in some tenebrionid beetles. J Exp Zool A Ecol Genet Physiol 176(2):137–145.  https://doi.org/10.1002/jez.1401760203 Google Scholar
  67. Tusé D, Miller MW (1984) Single-cell protein: current status and future prospects. Crit Rev Food Sci Nutr 19(4):273–325.  https://doi.org/10.1080/10408398409527379 CrossRefPubMedGoogle Scholar
  68. Ushida K, Kuriyama M (2006) Beta hydroxy short to medium chain fatty acid polymer. United States patent application US 10/570,133. 2006 Dec 7.Google Scholar
  69. Valentino F, Morgan-Sagastume F, Campanari S, Villano M, Werker A, Majone M (2017) Carbon recovery from wastewater through bioconversion into biodegradable polymers. New Biotechnol 37(Pt A):9–23.  https://doi.org/10.1016/j.nbt.2016.05.007 CrossRefGoogle Scholar
  70. Van Broekhoven S, Oonincx DG, Van Huis A, Van Loon JJ (2015) Growth performance and feed conversion efficiency of three edible mealworm species (Coleoptera: Tenebrionidae) on diets composed of organic by-products. J Insect Physiol 73:1–10.  https://doi.org/10.1016/j.jinsphys.2014.12.005 CrossRefPubMedGoogle Scholar
  71. Van Huis A, Van Itterbeeck J, Klunder H, Mertens E, Halloran A, Muir G, Vantomme P (2013) Edible insects: future prospects for food and feed security, vol 171. FAO Forestry, Rome, p 201Google Scholar
  72. Volova TG, Prudnikova SV, Boyandin AN (2016) Biodegradable poly-3-hydroxybutyrate as a fertiliser carrier. J Sci Food Agric 96(12):4183–4193.  https://doi.org/10.1002/jsfa.7621 CrossRefPubMedGoogle Scholar
  73. Waslien CI, Calloway DH (1969) Nutritional value of lipids in Hydrogenomonas eutropha as measured in the rat. Appl Microbiol 18(2):152–155PubMedPubMedCentralGoogle Scholar
  74. Weaver DK, McFarlane J (1990) The effect of larval density on growth and development of Tenebrio molitor. J Insect Physiol 36(7):531–536.  https://doi.org/10.1016/0022-1910(90)90105-O CrossRefGoogle Scholar
  75. Winston PW, Bates DH (1960) Saturated solutions for the control of humidity in biological research. Ecology 41(1):232–237.  https://doi.org/10.2307/1931961 CrossRefGoogle Scholar
  76. Wong Y-M, Brigham CJ, Rha C, Sinskey AJ, Sudesh K (2012) Biosynthesis and characterization of polyhydroxyalkanoate containing high 3-hydroxyhexanoate monomer fraction from crude palm kernel oil by recombinant Cupriavidus necator. Bioresour Technol 121:320–327.  https://doi.org/10.1016/j.biortech.2012.07.015 CrossRefPubMedGoogle Scholar
  77. Yang Y, Yang J, Wu W-M, Zhao J, Song Y, Gao L, Yang R, Jiang L (2015) Biodegradation and mineralization of polystyrene by plastic-eating mealworms: part 1. Chemical and physical characterization and isotopic tests. Environ Sci Technol 49(20):12080–12086.  https://doi.org/10.1021/acs.est.5b02661 CrossRefPubMedGoogle Scholar
  78. Zhang Y, Sun W, Wang H, Geng A (2013) Polyhydroxybutyrate production from oil palm empty fruit bunch using Bacillus megaterium R11. Bioresour Technol 147:307–314.  https://doi.org/10.1016/j.biortech.2013.08.029 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of Biological SciencesUniversiti Sains MalaysiaPenangMalaysia

Personalised recommendations