A novel biological recovery approach for PHA employing selective digestion of bacterial biomass in animals
- 438 Downloads
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.
KeywordsPolyhydroxyalkanoate Biological recovery Mealworms Selective digestion Small animals
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.
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.
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.
- 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
- 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
- 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
- Costa-Neto EM (2005) Entomotherapy, or the medicinal use of insects. J Ethnobiol 25(1):93–114.Google Scholar
- Doi Y (1990) Microbial polyesters. VCH, New YorkGoogle Scholar
- Dossey AT, Morales-Ramos JA, Rojas MG (2016) Insects as sustainable food ingredients: production, processing and food applications. Academic Press, CambridgeGoogle Scholar
- Gullan PJ, Cranston PS (2014) The insects: an outline of entomology. John Wiley & Sons, Chapman & Hall, OxfordGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Obreza TA, Rouse RE (2006) Long-term response of Hamlin’Orange trees to controlled-release nitrogen fertilizers. Hort Sci 41:423–426Google Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- Shaviv A (2005) Controlled release fertilizers. IFA International Workshop on Enhanced-Efficiency Fertilizers. Frankfurt. International Fertilizer Industry Association Paris, France, pp 28–30Google Scholar
- 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
- 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
- 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
- Trenkel ME (1997) Controlled-release and stabilized fertilizers in agriculture. Intl. Fert. Ind. Assn, ParisGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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