Abstract
Petroleum pollution is a major concern in Antarctica due to the persistent nature of its hydrocarbon components coupled with the region’s extreme environmental conditions, which means that bioremediation approaches are largely inapplicable at present. The current study assessed the ability of the psychrotolerant phenol-degrader, Rhodococcus sp. strain AQ5-07, to assimilate diesel fuel as the sole carbon source. Factors expected to influence the efficiency of diesel degradation, including the initial hydrocarbon concentration, nitrogen source concentration and type, temperature, pH and salinity were studied. Strain AQ5-07 displayed optimal cell growth and biodegradation activity at 1% v/v initial diesel concentration, 1 g/L NH4Cl concentration, pH 7 and 1% NaCl during one-factor-at-a-time (OFAT) analyses. Strain AQ5-07 was psychrotolerant based on its optimum growth temperature being near 20 °C. In conventionally optimised media, strain AQ5-07 showed total petroleum hydrocarbons (TPH) mineralisation of 75.83%. However, the optimised condition for TPH mineralisation predicted through statistical response surface methodology (RSM) enhanced the reduction to 90.39% within a 2 days incubation. Our preliminary data support strain AQ5-07 being a potential candidate for real-field soil bioremediation by specifically adopting sludge-phase bioreactor system in chronically cold environments such as Antarctica. The study also confirmed the utility of RSM in medium optimisation.
Similar content being viewed by others
References
Abbasian F, Palanisami T, Megharaj M, Naidu R, Lockington R, Ramadass K (2016) Microbial diversity and hydrocarbon degrading gene capacity of a crude oil field soil as determined by metagenomics analysis. Biotechnol Progr. https://doi.org/10.1002/btpr.2249
Acuna AJ, Pucci OH, Pucci GN (2012) Effect of nitrogen deficiency in the biodegradation of aliphatic and aromatic hydrocarbons in Patagonian contaminated soil. Int J Res Rev Appl Sci 11:470–476
Ahmad SA, Shukor MY, Shamaan NA, MacCormack WP, Syed MA (2013) Molybdate reduction to molybdenum blue by an Antarctic bacterium. BioMed Res Int. https://doi.org/10.1155/2013/871941
Aislabie JM, Balks MR, Foght JM, Waterhouse EJ (2004) Hydrocarbon spills on Antarctic soil: effect and management. Environ Sci Technol 38:1265–1274
Aislabie J, Saul DJ, Foght JM (2006) Bioremediation of hydrocarbon-contaminated polar soils. Extremophiles 10:171–179
Andersson BE, Lundstedt S, Tornberg K, Schnurer Y, Oberg LG, Mattiasson B (2003) Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting fungi and their effect on the indigenous soil bacteria. Environ Toxicol Chem 22:1238–1243
Arif NM, Ahmad SA, Syed MA, Shukor MY (2012) Isolation and characterisation of a phenol-degrading Rhodococcus sp. strain AQ5NOL 2 KCTC 11961BP. J Basic Microbiol 53:9–19
Atlas RM, Hazen TC (2011) Oil biodegradation and bioremediation: a tale of the two worst spills in U.S. history. Environ Sci Technol 45:6709–6715
Auffret M, Labbe D, Thouand G, Greer CW, Fayolle-Guichard F (2009) Degradation of a mixture of hydrocarbons, gasoline, and diesel oil additives by Rhodococcus aetherivorans and Rhodococcus wratislaviensis. Appl Environ Microbiol 75:7774–7782
Bas D, Boyaci IH (2007) Modeling and optimization I: usability of response surface methodology. J Food Eng 78:836–845
Bej AK, Saul D, Aislabie J (2000) Cold-tolerant alkane-degrading Rhodococcus species from Antarctica. Polar Biol 23:100–105
Beyer J, Jonsson G, Porte C, Krahn MM, Ariese F (2010) Analytical methods for determining metabolites of polycyclic aromatic hydrocarbon (PAH) pollutants in fish bile: a review. Environ Toxicol Pharmacol 30:224–244
Bhatnagar S, Kumari R (2013) Bioremediation: a sustainable tool for environmental management—a review. Annu Rev Res Biol 3:974–993
Boopathy R (2000) Factors limiting bioremediation technologies. Bioresour Technol 74:63–67
Box GEP, Wilson KB (1951) On the experimental attainment of optimum conditions. J R Stat Soc 13:1–45
Brito EMS, Guyoneaud R, Goni-Urriza M, Ranchou-Peyruse A, Verbaere A, Crapez MAC, Wasserman JCA, Duran R (2006) Characterisation of hydrocarbonoclastic bacterial communities from mangrove sediments in Guanabara Bay, Brazil. Res Microbiol 157:752–762
Bushnell LD, Haas HF (1941) The utilisation of certain hydrocarbons by microorganisms. J Bacteriol 41:653–673
Campbell IB, Claridge GGC, Campbell DI, Balks MR (1998) The soil environment. In: Priscu JC (ed) Ecosystem processes in a Polar Desert: The McMurdo Dry Valleys, Antarctica. Antarctic Research Series 72. American Geophysical Union, Washington, pp 97–322
Chikere CB, Okpokwasili GC, Chikere BO (2011) Monitoring of microbial hydrocarbon remediation in the soil. 3 Biotech 1:117–138
Convey P (2013) Antarctic ecosystems. In: Levin SA (ed) Encyclopedia of biodiversity, 2nd edn. Elsevier, San Diego, pp 179–188
Convey P, Coulson SJ, Worland MR, Sjöblom A (2018) The importance of understanding annual and shorter-term temperature patterns and variation in the surface levels of polar soils for terrestrial biota. Polar Biol 41:1587–1605
Curtosi A, Pelletier E, Vodopivez CL, Mac Cormack WP (2009) Distribution of PAHs in the water column, sediments and biota of Potter Cove, South Shetland Islands, Antarctica. Antarct Sci 21:329–339
de Carvalho CCCR (2012) Adaptation of Rhodococcus erythropolis cells for growth and bioremediation under extreme conditions. Res Microbiol 163:123–136
de Carvalho CCCR, Wick LY, Heipieper HJ (2009) Cell wall adaptations of planktonic and biofilm Rhodococcus erythropolis cells to growth on C5 to C16 n-alkane hydrocarbons. Appl Microbiol Biotechnol 82:311–320
de Jesus HE, Peixoto RS, Rosado AS (2015) Bioremediation in Antarctic soils. J Pet Environ Biotechnol 6:248. https://doi.org/10.4172/2157-7463.1000248
Foong CP, Vui Ling CMW, González M (2010) Metagenomic analyses of the dominant bacterial community in the Fildes Peninsula, King George Island (South Shetland Islands). Polar Sci 4:263–273
Frantzen M, Falk-Patersen I-B, Nahrgang J, Smith TJ, Olsen TH, Hangstad TA, Camus L (2012) Toxicity of crude oil and pyrene to the embryos of beach spawning capelin (Mallotus villosus). Aquat Toxicol 108:42–52
García-Borboroglu P, Boersma PD, Reyes L, Skewgar E (2008) Petroleum pollution and penguins: marine conservation tools to reduce the problem. In: Hofer TN (ed) Marine pollution: new research. Nova Science Publishers Inc., New York, pp 339–356
Habib S, Ahmad SA, Wan Johari WL, Shukor MY, Alias SA, Khalil KA, Yasid NA (2018) Evaluation of conventional and response surface level optimisation of n-dodecane (n-C12) mineralisation by psychrotolerant strains isolated from pristine soil at Southern Victoria Island, Antarctica. Microb Cell Fact 17:44. https://doi.org/10.1186/s12934-018-0889-8
Hasan SA, Jabeen S (2015) Degradation kinetics and pathway of phenol by Pseudomonas and Bacillus species. Biotechnol Biotechnol Equip 29:45–53
Ibrahim S, Shukor MY, Khalil KA, Halmi MIE, Syed MA, Ahmad SA (2015) Application of response surface methodology for optimising caffeine-degrading parameters by Leifsonia sp. strain SIU. J Environ Biol 36:1215–1221
Ismail W, Gescher J (2012) The epoxy coenzyme—a thioesters pathways for degradation of aromatic compounds. Appl Environ Microbiol 78:5043–5051
Jain PK, Gupta VK, Gaur RK, Lowry M, Jaroli D, Chauhan U (2011) Bioremediation of petroleum oil contaminated soil and water. Res J Environ Toxicol 5:1–26
Karamba KI, Ahmad SA, Zulkharnain A, Syed MA, Khalil KA, Shamaan NA, Dahalan FA, Shukor MY (2016) Optimisation of biodegradation conditions for cyanide removal by Serratia marcescens strain AQ07 using one-factor-at-a-time technique and response surface methodology. Rend Lincei 27:533. https://doi.org/10.1007/s12210-016-0516-8
Kuyukina MS, Ivshina IB, Makarov SO, Litvinenko LV, Cunningham CJ, Philp JC (2005) Effect of biosurfactants on crude oil desorption and mobilization in a soil system. Environ Int 31:155–161
Lachacz A, Kalisz B, Gielwanowska I, Olech M, Chwedorzewska KJ, Kellman-Sopyla W (2018) Nutrient abundance and variability from soils in the coast of King George Island. J Plant Nutr Soil Sci 18:294–311
Leahy JG, Colwell RR (1990) Microbial degradation of hydrocarbons in the environment. Microbiol Rev 54:305–315
Lee M, Kim MK, Singleton I, Goodfellow M, Lee S-T (2006) Enhanced biodegradation of diesel oil by a newly identified Rhodococcus baikonurensis EN3 in the presence of mycolic acid. J Appl Microbiol 100:325–333
Lee GLY, Ahmad SA, Yasid NA, Zulkharnain A, Convey P, Wan Johari WL, Alias SA, Gonzalez-Rocha G, Shukor MY (2018) Biodegradation of phenol by cold-adapted bacteria from Antarctic soils. Polar Biol 41:553–562
Lim MW, Lau EV, Poh PE (2016) A comprehensive guide of remediation technologies for oil contaminated soil—present works and future directions. Mar Pollut Bull 109:14–45
Liu C-W, Liu H-S (2011) Rhodococcus erythropolis strain NTU-1 efficiently degrades and traps diesel and crude oil in batch and fed-batch bioreactors. Process Biochem 46:202–209
Macaulay BM, Rees D (2014) Bioremediation of oil spills: a review of challenges for research advancement. Ann Environ Sci 8:9–37
MacLeod CT, Daugulis AJ (2005) Interfacial effects in a two-phase partitioning bioreactor: degradation of polycyclic aromatic hydrocarbons (PAHs) by a hydrophobic mycobacterium. Process Biochem 40:1799–1805
Manogaran M, Shukor MY, Yasid NA, Khalil KA, Ahmad SA (2018) Optimisation of culture composition for glyphosate degradation by Burkholderia vietnamiensis strain AQ5-12. 3 Biotech 8(2):108. https://doi.org/10.1007/s13205-018-1123-4
Margesin R, Moertelmaier C, Mair J (2013) Low-temperature biodegradation of petroleum hydrocarbons (n-alkanes, phenol, anthracene, pyrene) by four actinobacterial strains. Int Biodeterior Biodegrad 84:185–191
Mazuki TAT, Shukor MY, Ahmad SA (2019) Bioremediation of phenol in Antarctic: a mini review. Malays J Biochem Mol Biol 22:1–6
McIlvaine TC (1921) A buffer solution for colorimetric comparison. J Biol Chem 49:183–186
Michaud L, Lo Giudice A, Saitta M, De Dominico M, Bruni V (2004) The biodegradation efficiency on diesel oil by two psychrotrophic Antarctic marine bacteria during a two-month-long experiment. Mar Pollut Bull 49:405–409
Montone RC, Taniguchi S, Colabuono FI, Martins CC, Cipro CVZ, Barroso HS, da Silva J, Bicego MC, Weber RR (2015) Persistent organic pollutants and polycyclic aromatic hydrocarbons in penguins of the genus Pygoscelis in Admiralty Bay—an Antarctic specially managed area. Mar Pollut Bull 106:377–382
Moscoso F, Teijiz I, Deive FJ, Sanroman MA (2012) Efficient PAHs biodegradation by a microbial consortium at flask and bioreactor scale. Biores Technol 119:270–276
Mrozik A, Piotrowska-Seget Z (2010) Bioaugmentation as a strategy for cleaning up of soils contaminated with aromatic compounds. Microbiol Res 165:363–375
Muangchinda C, Chavanich S, Viyakarn V, Watanabe K, Imura S, Vangnai AS, Pinyakong O (2015) Abundance and diversity of functional genes involved in the degradation of aromatic hydrocarbons in Antarctic soils and sediments around Syowa Station. Environ Sci Pollut Res Int 22:4725–4735
Muller T, Walter B, Wirtz A, Burkovski A (2006) Ammonium toxicity in bacteria. Curr Microbiol 52:400–406
Nor NM, Mohamed MS, Loh TC, Foo HL, Rahim RA, Tan JS, Mohamad R (2017) Comparative analyses on medium optimization using one-factor-at-a-time, response surface methodology, and artificial neural network for lysine–methionine biosynthesis by Pediococcus pentosaceus RF-1. Biotechnol Biotechnol Equip 31:935–947
Plackett RL, Burman JP (1946) The design of optimum multifactorial experiments. Biometrika 33:305–325
Pruden A, Sedran M, Suidan M, Venosa A (2003) Biodegradation of MTBE and BTEX in an aerobic fluidized bed. Water Sci Technol 47:123–128
Prus W, Fabianska MJ, Labno R (2015) Geochemical markers of soil anthropogenic contaminants in polar scientific stations nearby (Antarctica, King George Island). Sci Total Environ 518–519:266–279
Qin X, Tang JC, Li DS, Zhang QM (2012) Effect of salinity on the bioremediation of petroleum hydrocarbons in a saline-alkaline soil. Lett Appl Microbiol 55:210–217
Rojo F (2009) Degradation of alkanes by bacteria. Environ Microb 11:2477–2490
Ruberto LAM, Vazquez S, Lobalbo A, MacCormack WP (2005) Psychrotolerant hydrocarbon-degrading Rhodococcus strains isolated from polluted Antarctic soils. Antarct Sci 17:47–56
Ryu HW, Yang HJ, Youn-Joo A, Kyung-Suk C (2006) Isolation and characterisation of psychrotrophic and halotolerant Rhodococcus sp. YHLT-2. J Microbiol Biotechnol 16:605–612
Shukor MY, Dahalan FA, Jusoh AZ, Muse R, Shamaan NA, Syed MA (2009) Characterisation of a diesel-degrading strain isolated from a hydrocarbon-contaminated site. J Environ Biol 30:145–150
Sikkema J, de Bont JA, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222
Speight JG (2014) The chemistry and technology of petroleum, 5th edn. CRC Press, Taylor & Francis Group, Boca Raton
Sun G, Zhang J, Li H (2014) Structural behaviour of waxy crude oil emulsion gels. Energy Fuels 28:3718–3729
Suzuki T, Yamaya S (2005) Removal of hydrocarbons in a rotating biological contactor with biodrum. Process Biochem 40:3429–3433
Szopinska M, Szuminska D, Bialik RJ, Dymerski T, Rosenberg E, Polkowska Z (2019) Determination of polycyclic aromatic hydrocarbons (PAHs) and other organic pollutants in freshwaters on the western shore of Admiralty Bay (King George Island, Maritime Antarctica). Environ Sci Pollut Res 26:18143–18161
Tyagi M, da Fonseca MMR, de Carvalho CCCR (2011) Bioaugmentation and biostimulation strategies to improve the effectiveness of bioremediation processes. Biodegradation 22:231–241
Van Hamme JD, Singh A, Ward PO (2003) Recent advances in petroleum microbiology. Microbiol Mol Biol Rev 67:503–549
Vazquez S, Monien P, Minetti RP, Jurgens J, Curtosi A, Primitz JV, Frickenhaus S, Abele D, MacCormack W, Helmke E (2017) Bacterial communities and chemical parameters in soils and coastal sediments in response to diesel spills at Carlini Station, Antarctica. Sci Total Environ 606:26–37
Wang L, Camus AC, Dong W, Thornton C, Willet KL (2010) Expression of CYP1C1 and CYP1A in Fundulus heteroclitus during PAH-induced carcinogenesis. Aquat Toxicol 99:439–447
Waterhouse EJ (2001) Ross Sea region 2001: a state of the environment report for the Ross Sea region of Antarctica, chapter 2. New Zealand Antarctic Institute (Antarctica New Zealand), Christchurch, NZ
Yao Y, Meng X-Z, Wu C-C, Bao L-J, Wang F, Wu F-C, Zeng EY (2016) Tracking human footprints in Antarctica through passive sampling of polycyclic aromatic hydrocarbons in inland lakes. Environ Pollut 213:412–419
Yusuf I, Ahmad SA, Phang LY, Syed MA, Shamaan NA, Abdul Khalil K, Dahalan FA, Shukor MY (2016) Keratinase production and biodegradation of polluted secondary chicken feather wastes by a newly isolated multi heavy metal tolerant bacterium-Alcaligenes sp. AQ05-001. J Environ Manage 183:182–195
Acknowledgements
This project was financially supported by Putra‒IPM fund under the research grant attached to S.A. Ahmad (GP-Matching Grant/2016/9300430, GP-Matching Grant/2017/9300436, GPM-2018/9660000 and GPM-2019/ 9678900) disbursed by Universiti Putra Malaysia (UPM) and YPASM Smart Partnership Initiative by Sultan Mizan Antarctic Research Foundation (YPASM). P. Convey is supported by NERC core funding to the BAS ‘Biodiversity, Ecosystems and Adaptation’ Team. C.G. Fuentes is supported by Centro de Investigacion y Monitoreo Ambiental Antàrctico (CIMAA) Project. The authors would like to thank Assoc. Prof. Dr. Siti Aisyah Alias from University of Malaya, Malaysia and Professor Gerardo Gonzalez-Rocha from Universidad de Concepcion for the help of the first study. The authors also would like to thank Chilean Army and the Antarctic General Bernardo O'Higgins Station staff, Instituto Antártico Chileno (INACH) and National Antarctic Research Centre (NARC). We also thank the Public Service Department of Malaysia (JPA) for granting a master programme scholarship to Ahmad Fareez Ahmad Roslee.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Driessen.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Roslee, A.F.A., Zakaria, N.N., Convey, P. et al. Statistical optimisation of growth conditions and diesel degradation by the Antarctic bacterium, Rhodococcus sp. strain AQ5‒07. Extremophiles 24, 277–291 (2020). https://doi.org/10.1007/s00792-019-01153-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-019-01153-0