Abstract
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.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig4_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig5_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs13205-019-1574-2/MediaObjects/13205_2019_1574_Fig6_HTML.png)
Similar content being viewed by others
References
Abarca-Guerrero L, Maas G, Hogland W (2013) Solid waste management challenges for cities in developing countries. Waste Manag 33:220–232. https://doi.org/10.1016/j.wasman.2012.09.008
Abbasian F, Lockington R, Mallavarapu M, Naidu R (2015) A comprehensive review of aliphatic hydrocarbon biodegradation by bacteria. Appl Biochem Biotechnol 176:670–699. https://doi.org/10.1007/s12010-015-1603-5
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 185–206
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. https://doi.org/10.1016/j.enconman.2017.11.004
Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642. https://doi.org/10.1007/s00253-009-2355-3
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. https://doi.org/10.1515/ijcre-2017-0206
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. https://doi.org/10.3303/CET1543047
Food and Agriculture Organization (2015) Perdidas y desperdicios de alimentos en América latina y el Caribe. http://www.fao.org/3/a-i4655s.pdf. Accessed 30 Jan 2018
Heller WP, Kissinger KR, Matsumoto TK, Keith LM (2015) Utilization of papaya waste and oil production by Chlorella protothecoides. Algal Res 12:156–160. https://doi.org/10.1016/j.algal.2015.08.013
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. https://doi.org/10.1016/j.biotechadv.2012.08.010
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. https://doi.org/10.1016/j.jbiotec.2018.07.039
Kapello GE (2017) Microbial strategies for oil biodegradation. In: Becker SM (ed) Modelling of microscale transport in biological processes. Academic Press, New York, pp 19–39
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. https://doi.org/10.1021/es203552p
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. https://doi.org/10.3390/ijms16034814
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. https://doi.org/10.1016/j.cej.2012.01.114
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. https://doi.org/10.1080/19443994.2013/876670
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. https://doi.org/10.1590/S0101-20612011000400016
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. https://doi.org/10.1016/j.wasman.2015.09.009
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. https://doi.org/10.5004/dwt.2017.21307
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. https://doi.org/10.1007/s00449-018-1920-5
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. https://doi.org/10.1111/j.1745-4522.2005.00006.x
Rhodes CJ (2014) Mycoremediation (bioremediation with fungi)—growing mushrooms to clean the earth. Chem Spec Bioavailab 26:196–198. https://doi.org/10.3184/095422914X14047407349335
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 2:50–55
Secretaría de Agricultura, G, Rural D, Pesca y Alimentación (2018) Servicio de Información Agroalimentaria y Pesquera. http://infosiap.siap.gob.mx/aagricola_siap_gb/icultivo/index.jsp. Accessed 5 Jan 2018
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. https://doi.org/10.1016/jclepro.2017.08.021
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 17:256–266
Thapa B, KC AK, Ghimire A (2012) A review on bioremediation of petroleum hydrocarbon contaminants. Soil J Sci Eng Technol 8:164–170. https://doi.org/10.3126/kuset.v8i1.6056
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. https://doi.org/10.1016/j.ibiod.2012.01.009
Von Bertalanffy L (1938) A quantitative theory of organic growth (inquiries on growth laws II). Hum Biol 10:181–213
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. https://doi.org/10.1073/pnas.1118029109
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. https://doi.org/10.3390/ijms19041114
Zwietering MH, Jongenburger I, Rombouts FM, Van’T, Riet K (1990) Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875–1881
Acknowledgements
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
On behalf of all authors, the corresponding author states that there are no conflicts of interest.
Rights and permissions
About this article
Cite this article
Valdivia-Rivera, S., Varela-Santos, E.d., Quiñones-Muñoz, T.A. et al. Production of hydrocarbon-degrading microorganisms using agricultural residues of Mangifera indica L. and Carica papaya as carbon source. 3 Biotech 9, 43 (2019). https://doi.org/10.1007/s13205-019-1574-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-019-1574-2