3 Biotech

, 9:43 | Cite as

Production of hydrocarbon-degrading microorganisms using agricultural residues of Mangifera indica L. and Carica papaya as carbon source

  • Sergio Valdivia-Rivera
  • Elizabeth del Carmen Varela-Santos
  • Tannia Alexandra Quiñones-Muñoz
  • Ricardo Hernández-Martínez
  • Manuel Alejandro Lizardi-JiménezEmail author
Original Article


The aim of the present study was to evaluate the potential of oils from agricultural residues, such as Mangifera indica L. (mango) and Carica papaya (papaya) from the Papaloapan region, Mexico, as a carbon source for the production of hydrocarbon-degrading (hydrocarbonoclastic) microorganisms in an airlift bioreactor via a common metabolic pathway for hydrocarbons and fatty acids. Biomass growth and carbon source uptake were measured using optical density and gas chromatography, respectively. Gompertz, logistic, and Von Bertalanffy mathematical models were used to obtain kinetic parameters such as the lag phase, maximum specific growth, and consumption rate. The hydrocarbonoclastic consortium was able to grow using papaya (6.09 ± 0.23 g L−1) and mango (2.59 ± 0.30 g L−1) oils, which contain certain antibacterial fatty acids. Differences observed in maximum specific growth and consumption rates indicate that, although mango oil was consumed faster (0.33 day−1 for mango and 0.25 day−1 for papaya), papaya oil provided a higher rate of biomass production per microorganism (0.24 day−1 for mango and 0.44 day−1 for papaya). Additionally, the consortium was able to consume 13 g L−1 diesel as a sole carbon source and improve its maximum specific consumption rate following growth using the oils. Furthermore, the maximum specific growth rate was decreased, indicating a change in the consortium capabilities. Nevertheless, agricultural waste oils from the Papaloapan region can be used to cultivate hydrocarbonoclastic microorganisms. The present study creates the possibility of investigating carbon sources other than hydrocarbons for the production of hydrocarbonoclastic microorganisms.


Hydrocarbonoclastic microorganisms Mangifera indica L. Carica papaya Hydrocarbon pollution Mathematical modelling 



This work was supported by the National Council of Science and Technology under Grants: 288099 INFR-2016-1; Cátedras-CONACYT (ITSTB 694); and CONACYT National Scholarship (594786) for the first author.

Compliance with ethical standards

Conflict of interest

On behalf of all authors, the corresponding author states that there are no conflicts of interest.


  1. Abarca-Guerrero L, Maas G, Hogland W (2013) Solid waste management challenges for cities in developing countries. Waste Manag 33:220–232. CrossRefGoogle Scholar
  2. Abbasian F, Lockington R, Mallavarapu M, Naidu R (2015) A comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Appl Biochem Biotechnol 176:670–699. CrossRefPubMedGoogle Scholar
  3. Abha S, Swaranjit C (2012) Hydrocarbon pollution: effects on living organisms, remediation of contaminated environments, and effects of heavy metals co-contamination on bioremediation. In: Romero-Zerón L (ed) Introduction to enhanced oil recovery (EOR) processes and bioremediation of oil-contaminated sites. InTech, Rijeka, pp 185–206Google Scholar
  4. Anwar M, Rasul MG, Aswath N (2018) Production optimization and quality assessment of papaya (Carica papaya) biodiesel with response surface methodology. Energy Convers Manag 156:103–112. CrossRefGoogle Scholar
  5. Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642. CrossRefPubMedGoogle Scholar
  6. Dutta A, Valdivia-Rivera S, Lizardi-Jiménez MA (2018) Simultaneous diesel and oxygen transfer rate on the production of an oil-degrading consortium in an airlift bioreactor: high-dispersed phase concentration. Int J Chem React Eng. CrossRefGoogle Scholar
  7. Ehrhardt DD, Secato JFF, Tambourgi EB (2015) Biosurfactant production by bacillus subtilis using the residue from processing of pineapple, enriched with glycerol, as substrate. Chem Eng Trans 43:277–282. CrossRefGoogle Scholar
  8. Food and Agriculture Organization (2015) Perdidas y desperdicios de alimentos en América latina y el Caribe. Accessed 30 Jan 2018
  9. Heller WP, Kissinger KR, Matsumoto TK, Keith LM (2015) Utilization of papaya waste and oil production by Chlorella protothecoides. Algal Res 12:156–160. CrossRefGoogle Scholar
  10. Huang C, Chen X, Xiong L, Chen XD, Ma LL, Chen Y (2013) Single cell oil production from low-cost substrates: the possibility and potential of its industrialization. Biotechnol Adv 31:129–139. CrossRefPubMedGoogle Scholar
  11. Kadri T, Magdouli S, Rouissi T, Brar SK, Daghrir R, Lauzon JM (2018) Bench-scale production of enzymes from the hydrocarbonoclastic bacteria Alcanivorax borkumensis and biodegradation tests. J Biotechnol 283:105–114. CrossRefPubMedGoogle Scholar
  12. Kapello GE (2017) Microbial strategies for oil biodegradation. In: Becker SM (ed) Modelling of microscale transport in biological processes. Academic Press, New York, pp 19–39CrossRefGoogle Scholar
  13. Lin Q, Mendelssohn IA (2012) Impacts and recovery of the deepwater horizon oil spill on vegetation structure and function of coastal salt marshes in the Northern Gulf of Mexico. Environ Sci Technol 46:3737–3743. CrossRefPubMedGoogle Scholar
  14. Liu JF, Mbadinga SM, Yang SZ, Gu JD, Mu BZ (2015) Chemical structure, property and potential applications of biosurfactants produced by Bacillus subtilis in petroleum recovery and spill mitigation. Int J Mol Sci 16:4814–4837. CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lizardi-Jiménez MA, Saucedo-Castañeda G, Thalasso F, Gutiérrez-Rojas M (2012) Simultaneous hexadecane and oxygen transfer rate on the production of an oil-degrading consortium in a three-phase airlift bioreactor. Chem Eng J 187:160–165. CrossRefGoogle Scholar
  16. Lizardi-Jiménez MA, Leal-Bautista RM, Ordaz A, Reyna-Velarde R (2013) Airlift bioreactors for hydrocarbon water pollution remediation in a tourism development pole. Desalin Water Treat 54:44–49. CrossRefGoogle Scholar
  17. Malacrida CR, Kimura M, Jorge N (2011) Characterization of a high oleic oil extracted from papaya (Carica papaya L.) seeds. Food Sci Technol 31:929–934. CrossRefGoogle Scholar
  18. Miezah K, Obiri-Danso K, Kádár Z, Fei-Baffoe B, Mensah MY (2015) Municipal solid waste characterization and quantification as a measure towards effective waste management in Ghana. Waste Manag 46:15–27. CrossRefPubMedGoogle Scholar
  19. Nápoles-Álvarez J, Ábalos-Rodríguez A, Rodríguez-Pérez S, Sánchez-Vázquez V, Gutiérrez-Rojas M (2017) Airlift bioreactor using a bacterial mixed culture improves hydrocarbon degradation in contaminated salty water. Desalin Water Treat 86:28–34. CrossRefGoogle Scholar
  20. Ortega-de la Rosa ND, Vázquez-Vázquez JL, Huerta-Ochoa S, Gimeno M, Gutiérrez-Rojas M (2018) Stable bioemulsifiers are produced by Acinetobacter bouvetii UAM25 growing in different carbon sources. Bioprocess Biosyst Eng 41:859–869. CrossRefPubMedGoogle Scholar
  21. Puangsri T, Abdulkarim SM, Ghazali HM (2004) Properties of Carica papaya L. (papaya) seed oil following extractions using solvent and aqueous enzymatic methods. J Food Lipids 12:62–76. CrossRefGoogle Scholar
  22. Rhodes CJ (2014) Mycoremediation (bioremediation with fungi)—growing mushrooms to clean the earth. Chem Spec Bioavailab 26:196–198. CrossRefGoogle Scholar
  23. Santisi S, Genovese M, Crisafi F, Gentile G, Volta A, Bonsignore M, Cappello S (2015) Effects of growth conditions on hydrophobicity in marine obligate hydrocarbonoclastic bacteria. Int J Microbiol Appl 2:50–55Google Scholar
  24. Secretaría de Agricultura, G, Rural D, Pesca y Alimentación (2018) Servicio de Información Agroalimentaria y Pesquera. Accessed 5 Jan 2018
  25. Soto-Oñate D, Caballero G (2017) Oil spills, governance and institutional performance: the 1992 regime of liability and compensation for oil pollution damage. J Clean Prod 166:299–311. CrossRefGoogle Scholar
  26. Tapia-Santos M, Perez-Armendáriz B, Cavazos-Arroyo J, Mayett-Moreno Y (2013) Obtención de aceite de semilla de mango manila (Mangifera indica L.) como una alternativa para aprovechar subproductos agroindustriales en regiones tropicales. Rev Mex Agronegocios 17:256–266Google Scholar
  27. Thapa B, KC AK, Ghimire A (2012) A review on bioremediation of petroleum hydrocarbon contaminants. Soil J Sci Eng Technol 8:164–170. CrossRefGoogle Scholar
  28. Tzintzun-Camacho O, Loera O, Ramírez-Saad HC, Gutiérrez-Rojas M (2012) Comparison of mechanisms of hexadecane uptake among pure and mixed cultures derived from a bacterial consortium. Int Biodeterior Biodegrad 70:1–7. CrossRefGoogle Scholar
  29. Von Bertalanffy L (1938) A quantitative theory of organic growth (inquiries on growth laws II). Hum Biol 10:181–213Google Scholar
  30. White HK, Hsing P, Cho W, Shank TM, Cordes EE, Quattrini AM, Nelson RK, Camilli R, Demopoulos AWJ, German CR, Brooks JM, Roberts HH, Shedd W, Reddy CM, Fisher CR (2012) Impact of the deepwater horizon oil spill on a deep-water coral community in the Gulf of Mexico. PNAS 109:20303–20308. CrossRefPubMedGoogle Scholar
  31. Yoon BK, Jackman JA, Valle-González ER, Cho NJ (2018) Antibacterial free fatty acids and monoglycerides: biological activities, experimental testing, and therapeutic applications. Int J Mol Sci 19:1114. CrossRefPubMedCentralGoogle Scholar
  32. Zwietering MH, Jongenburger I, Rombouts FM, Van’T, Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881PubMedPubMedCentralGoogle Scholar

Copyright information

© King Abdulaziz City for Science and Technology 2019

Authors and Affiliations

  1. 1.Instituto Tecnológico Superior de Tierra BlancaMexicoMexico
  2. 2.CONACYT-Instituto Tecnológico Superior de Tierra BlancaMexicoMexico

Personalised recommendations