Browse > Article
http://dx.doi.org/10.4014/mbl.1911.11014

Rhizoremdiation of Petroleum Hydrocarbon-contaminated Soils and Greenhouse Gas Emission Characteristics: A Review  

Seo, Yoonjoo (Department of Environmental Science and Engineering, Ewha Womans University)
Cho, Kyung-Suk (Department of Environmental Science and Engineering, Ewha Womans University)
Publication Information
Microbiology and Biotechnology Letters / v.48, no.2, 2020 , pp. 99-112 More about this Journal
Abstract
Rhizoremediation, based on the ecological synergism between plant and rhizosphere microorganisms, is an environmentally friendly method for the remediation of petroleum hydrocarbon-contaminated soils. In order to mitigate global climate change, it is necessary to minimize greenhouse gas emissions while cleaning-up contaminated soils. In rhizoremediation, the main factors affecting pollutant remediation efficiency and greenhouse gas emissions include not only pollutant and soil physicochemical properties, but also plant-microbe interactions, microbial activity, and addition of amendments. This review summarizes the development in rhizoremediation technology for purifying oil-contaminated soils. In addition, the key parameters and strategies required for rhizoremediation to mitigate climate change mediation are discussed.
Keywords
Rhizoremediation; petroleum hydrocarbon; contaminated soil; plant; rhizomicroorganism; greenhouse gas mitigation;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Hussain I, Puschenreiter M, Gerhard S, Schoftner P, Yousaf S, Wang A, et al. 2018. Rhizoremediation of petroleum hydrocarbon-contaminated soils: Improvement opportunities and field applications. Environ. Exp. Bot. 147: 202-219.   DOI
2 Varjani SJ. 2017. Microbial degradation of petroleum hydrocarbons. Bioresour. Technol. 223: 277-286.   DOI
3 Ron EZ, Rosenberg E. 2014. Enhanced bioremediation of oil spills in the sea. Curr. Opin. Biotechnol. 27: 191-194.   DOI
4 Aisien FA, Chiadikobi JC, Aisien ET. 2009. Toxicity assessment of some crude oil contaminated soils in the Niger delta. Adv. Mater. Res. 62-64: 451-455.   DOI
5 Hentati O, Lachhab R, Ayadi M, Ksibi M. 2013. Toxicity assessment for petroleum-contaminated soil using terrestrial invertebrates and plant bioassays. Environ. Monit. Assess. 185: 2989-2998.   DOI
6 Martin BC, George SJ, Price CA, Ryan MH, Tibbett M. 2014. The role of root exuded low molecular weight organic anions in facilitating petroleum hydrocarbon degradation: current knowledge and future directions. Sci. Total Environ. 472: 642-653.   DOI
7 Kaimi E, Mukaidani T, Miyoshi S, Tamaki M. 2006. Ryegrass enhancement of biodegradation in diesel-contaminated soil. Environ. Pollut. 55: 110-119.
8 Nanekar S, Dhote M, Kashyap S, Singh SK, Juwarkar AA. 2015. Microbe assisted phytoremediation of oil sludge and role of amendments: a mesocosm study. Int. J. Environ. Sci. Technol. 12: 193-202.   DOI
9 Basumatary B, Bordoloi S, Sarma HP. 2012. Crude oil-contaminated soil phytoremediation by using Cyperus brevifolius (Rottb.) Hassk. Water Air Soil Pollut. 223: 3373-3383.   DOI
10 Singha LP, Sinha N, Pandey P. 2018. Rhizoremediation prospects of polyaromatic hydrocarbon degrading rhizobacteria, that facilitate glutathione and glutathione-S-transferase mediated stress response, and enhance growth of rice plants in pyrene contaminated soil. Ecotox. Environ. Safe. 164: 579-588.   DOI
11 Gao Y, Zong J, Que H, Zhou Z, Xiao M, Chen S. 2017. Inoculation with arbuscular mycorrhizal fungi increases glomalin-related soil protein content and PAH removal in soils planted with Medicago sativa L. Soil Biol. Biochem. 115: 148-151.   DOI
12 Liu W, Hou J, Wang Q, Ding L, Luo Y. 2014. Isolation and characterization of plant growth-promoting rhizobacteria and their effects on phytoremediation of petroleum-contaminated saline-alkali soil. Chemosphere 117: 303-308.   DOI
13 Agnello AC, Bagard M, van Hullebusch ED, Esposito G, Huguenot D. 2016. Comparative bioremediation of heavy metals and petroleum hydrocarbons co-contaminated soil by natural attenuation, phytoremediation, bioaugmentation and bioaugmentation-assisted phytoremediation. Sci. Total Environ. 563-564: 693-703.   DOI
14 Godheja J, Shekhar SK, Modi DR. 2017. Bacterial Rhizoremediation of Petroleum Hydrocarbons (PHC). In Plant-microbe interactions in agro-ecological perspectives. pp. 495-519. Springer, Singapore.
15 Sujatha N, Ammani K. 2013. Siderophore production by the isolates of fluorescent pseudomonads. Int. J. Curr. Res. Rev. 5: 1-7.
16 Ramadass K, Megharaj M, Venkateswarlu K, Naidu R. 2015. Ecological implications of motor oil pollution: earthworm survival and soil health. Soil Biol. Biochem. 85: 72-81.   DOI
17 Zaidi A, Khan MS, Ahemad M, Oves M. 2009. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol. Immunol. Hung. 56: 263-284.   DOI
18 Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA. 2013. Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springer Plus 2: 587.   DOI
19 Hall JA, Peirson D, Ghosh S, Glick BR. 1996. Root elongation in various agronomic crops by the plant growth promoting rhizobacterium Pseudomonas putida GR12-2. Isr. J. Plant Sci. 44: 37-42.   DOI
20 Safronova VI, Stepanok VV, Engqvist GL, Alekseyev YV, Belimov AA. 2006. Root-associated bacteria containing 1-aminocyclopropane-1-carboxylate deaminase improve growth and nutrient uptake by pea genotypes cultivated in cadmium supplemented soil. Biol. Fertil. Soils 42: 267-272.   DOI
21 Guan LL, Kanoh K, Kamino K. 2001. Effect of exogenous siderophores on iron uptake activity of marine bacteria under iron limited conditions. Appl. Environ. Microbiol. 67: 1710-1717.   DOI
22 Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, Zhang LX. 2004. Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biol. Control 29: 66-72.   DOI
23 Raj SN, Deepak SA, Basavaraju P, Shetty HS, Reddy MS, Kloepper JW. 2003. Comparative performance of formulations of plant growth promoting rhizobacteria in growth promotion and suppression of downy mildew in pearl millet. Crop Prot. 22: 579-588.   DOI
24 Cartmill AD, Cartmill DL, Alarcon A. 2014. Controlled release fertilizer increased phytoremediation of petroleum-contaminated sandy soil. Int. J. Phytoremediat. 16: 285-301.   DOI
25 Wiszniewska A, Hanus-Fajerska E, Muszynska E, Ciarkowska K. 2016. Natural organic amendments for improved phytoremediation of polluted soils: a review of recent progress. Pedosphere 26: 1-12.   DOI
26 Ameloot N, Graber ER, Verheijen FG, De Neve S. 2013. Interactions between biochar stability and soil organisms: review and research needs. Eur. J. Soil Sci. 64: 379-390.   DOI
27 Bisht S, Pandey P, Kaur G, Aggarwal H, Sood A, Sharma S, et al 2014. Utilization of endophytic strain Bacillus sp. SBER3 for biodegradation of polyaromatic hydrocarbons (PAH) in soil model system. Eur. J. Soil Biol. 60: 67-76.   DOI
28 Gopalakrishnan S, Srinivas V, Samineni S. 2017. Nitrogen fixation, plant growth and yield enhancements by diazotrophic growth-promoting bacteria in two cultivars of chickpea (Cicer arietinum L.). Biocatal. Agric. Biotechnol. 11: 116-123.   DOI
29 Hussain F, Hussain I, Khan AHA, Muhammad YS, Iqbal M, Soja G, et al. 2018. Combined application of biochar, compost, and bacterial consortia with Italian ryegrass enhanced phytoremediation of petroleum hydrocarbon contaminated soil. Environ. Exp. Bot. 153: 80-88.   DOI
30 Arslan M, Afzal M, Amin I, Iqbal S, Khan QM. 2014. Nutrients can enhance the abundance and expression of alkane hydroxylase CYP153 gene in the rhizosphere of ryegrass planted in hydrocarbon-polluted soil. PLoS One 9: e111208.   DOI
31 Pangala SR, Moore S, Hornibrook ERC, Gauci V. 2013. Trees are major conduits for methane egress from tropical forested wetlands. New Phytologist 197: 524-531.   DOI
32 Fatima K, Imran A, Naveed M, Afzal M. 2017. Plant-bacteria synergism: An innovative approach for the remediation of crude oil-contaminated soils. Soil Environ. 36: 93-113.   DOI
33 Plociniczak T, Fic E, Pacwa-Plociniczak M, Pawlik M, Piotrowska-Seget Z. 2017. Improvement of phytoremediation of an aged petroleum hydrocarbon-contaminated soil by Rhodococcus erythropolis CD 106 strain. Int. J. Phytoremediat. 19: 614-620.   DOI
34 Afegbua SL, Batty LC. 2019. Effect of plant growth promoting bacterium; Pseudomonas putida UW4 inoculation on phytoremediation efficacy of monoculture and mixed culture of selected plant species for PAH and lead spiked soils. Int. J. Phytoremediat. 21: 200-208.   DOI
35 Moubasher HA, Hegazy AK, Mohamed NH, Moustafa YM, Kabiel HF, Hamad AA. 2015. Phytoremediation of soils polluted with crude petroleum oil using Bassia scoparia and its associated rhizosphere microorganisms. Int. Biodeterior. Biodegr. 98: 113-120.   DOI
36 Emmanuel O, Enobong E, Gideon, A. 2018. Laboratory-scale bioremediation of crude oil polluted soil using a consortia of rhizobacteria obtained from plants in Gokana-Ogoni, Rivers state. J. Advan. Microbiol. 9: 2456-7116.
37 Leahy JG, Colwell RR. 1990. Microbial degradation of hydrocarbons in the environment. Microbiol. Mol. Biol. Rev. 54: 305-315.
38 Tremblay J, Yergeau E, Fortin N, Cobanli S, Elias M, King TL, et al. 2017. Chemical dispersants enhance the activity of oil-and gas condensate-degrading marine bacteria. ISME J. 11: 2793.   DOI
39 Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM. 2008. Root exudates regulate soil fungal community composition and diversity. Appl. Environ. Microbiol. 74: 738-744.   DOI
40 Salanitro JP. 2001. Bioremediation of petroleum hydrocarbons in soil. Adv. Agron. 72: 53-105.
41 Huang H, Tang J, Niu Z, Giesy JP. 2019. Interactions between electrokinetics and rhizoremediation on the remediation of crude oil-contaminated soil. Chemosphere 229: 418-425.   DOI
42 Pant R, Pandey P, Kotoky R. 2016. Rhizosphere mediated biodegradation of 1,4-dichlorobenzene by plant growth promoting rhizobacteria of Jatropha curcas. Ecol. Eng. 94: 50-56.   DOI
43 Logeshwaran P, Megharaj M, Chadalavada S, Bowman M, Naidu R. 2018. Petroleum hydrocarbons (PH) in groundwater aquifers: An overview of environmental fate, toxicity, microbial degradation and risk-based remediation approaches. Environ. Technol. Innov. 10: 175-193.   DOI
44 Liu PWG, Chang TC, Whang LM, Kao CH, Pan PT, Cheng SS. 2011. Bioremediation of petroleum hydrocarbon contaminated soil: effects of strategies and microbial community shift. Int. Biodeterior. Biodegr. 65: 1119-1127.   DOI
45 Cai B, Ma J, Yan G, Dai X, Li M, Guo S. 2016. Comparison of phytoremediation, bioaugmentation and natural attenuation for remediating saline soil contaminated by heavy crude. Biochem. Eng. J. 112: 170-177.   DOI
46 Nwinyi OC, Olawore YA. 2017. Biostimulation of spent engine oil contaminated soil using Ananas comosus and Solanum tuberosum peels. Environ. Technol. Innov. 8: 373-388.   DOI
47 Osterreicher-Cunha P, Vargas EA, Guimaraes JRD, Campos TMP, Nunes CMF, Costa A, et al. 2004. Evaluation of bioventing on a gasoline-ethanol contaminated undisturbed residual soil. J. Hazard. Mater. 110: 63-76.   DOI
48 Zhang X, Chen L, Liu X, Wang C, Chen X, Xu G, et al. 2014. Synergic degradation of diesel by Scirpus triqueter and its endophytic bacteria. Environ. Sci. Pollut. Res. 21: 8198-8205.   DOI
49 Insunza V, Alstrom S, Eriksson KB. 2002. Root bacteria from nematicidal plants and their biocontrol potential against trichodorid nematodes in potato. Plant Soil 241: 271-278.   DOI
50 Tara N, Afzal M, Ansari TM, Tahseen R, Iqbal S, Khan QM. 2014. Combined use of alkane-degrading and plant growth-promoting bacteria enhanced phytoremediation of diesel contaminated soil. Int. J. Phytoremediation 16: 1268-1277.   DOI
51 Wu T, Xu J, Xie W, Yao Z, Yang H, Sun C, et al. 2018. Pseudomonas aeruginosa L10: A hydrocarbon-degrading, biosurfactant-producing, and plant-growth-promoting endophytic bacterium isolated from a reed (Phragmites australis). Front. Microbiol. 9: 1087.   DOI
52 Gao Y, Guo S, Wang J, Li D, Wang H, Zeng D. 2014. Effects of different remediation treatments on crude oil contaminated saline soil. Chemosphere 117: 486-493.   DOI
53 Ebadi A, Sima NAK, Olamaee M, Hashemi M, Nasrabadi RG. 2018. Remediation of saline soils contaminated with crude oil using the halophyte Salicornia persica in conjunction with hydrocarbon-degrading bacteria. J. Environ. Manage. 219: 260-268.   DOI
54 Kerdchoechuen O. 2005. Methane emission in four rice varieties as related to sugars and organic acids of roots and root exudates and biomass yield. Agr. Ecosyst. Environ. 108: 155-163.   DOI
55 Silva IR, Novais RF, Jham GN, Barros NF, Gebrim FO, Nunes FN, et al. 2004. Responses of eucalypt species to aluminum: the possible involvement of low molecular weight organic acids in the Al tolerance mechanism. Tree Physiol. 24: 1267-1277.   DOI
56 Strom L, Owen AG, Godbold DL, Jones DL. 2002. Organic acid mediated P mobilization in the rhizosphere and uptake by maize roots. Soil Biol. Biochem. 34: 703-710.   DOI
57 Coskun D, Britto DT, Shi W, Kronzucker HJ. 2017. How plant root exudates shape the nitrogen cycle. Trends Plant Sci. 22: 661-673.   DOI
58 Bertola M, Mattarozzi M, Sanangelantoni AM, Careri M, Visioli G. 2019. PGPB colonizing three-year biochar-amended soil: Towards biochar-mediated biofertilization. J. Soil Sci. Plant Nut. 19: 841-850.   DOI
59 Yu XZ, Wu SC, Wu FY, Wong MH. 2011. Enhanced dissipation of PAHs from soil using mycorrhizal ryegrass and PAH-degrading bacteria. J. Hazard. Mater. 186: 1206-1217.   DOI
60 He J, Fana X, Liu H, He X, Wang Q, Liu Y, et al. 2019. The study on Suaeda heteroptera Kitag, Nereis succinea and bacteria's joint bioremediation of oil-contaminated soil. Microchem. J. 147: 872-878.   DOI
61 Shahzad A, Saddiqui S, Bano A. 2016. The response of maize (Zea mays L.) plant assisted with bacterial consortium and fertilizer under oily sludge. Int. J. Phytoremediat. 18: 521-526.   DOI
62 Hernandez-Ortega HA, Alarcon A, Ferrera-Cerrato R, Zavaleta-Mancera HA, Lopez-Delgado HA, Mendoza-Lopez MR. 2012. Arbuscular mycorrhizal fungi on growth, nutrient status, and total antioxidant activity of Melilotus albus during phytoremediation of a diesel-contaminated substrate. J. Environ. Econom. Manage. 95: S319-S324.
63 Hou J, Liu W, Wang B, Wang Q, Luo Y, Franks AE. 2015. PGPR enhanced phytoremediation of petroleum contaminated soil and rhizosphere microbial community response. Chemosphere 138: 592-598.   DOI
64 Hall J, Soole K, Bentham R. 2011. Hydrocarbon phytoremediation in the family Fabacea -a review. Int. J. Phytoremediat. 13: 317-332.   DOI
65 Fu D, Teng Y, Luo Y, Tu C, Li S, Li Z, et al. 2012. Effects of alfalfa and organic fertilizer on benzo[a]pyrene dissipation in an aged contaminated soil. Environ. Sci. Pollut. Res. 19: 1605-1611.   DOI
66 Riskuwa-Shehu ML, Ijah UJJ, Manga SB, Bilbis LS. 2017. Evaluation of the use of legumes for biodegradation of petroleum hydrocarbons in soil. Int. J. Environ. Sci. Technol. 14: 2205-2214.   DOI
67 Barati M, Bakhtiari F, Mowla D, Safarzadeh S. 2017. Total petroleum hydrocarbon degradation in contaminated soil as affected by plants growth and biochar. Environ. Earth Sci. 76: 688.   DOI
68 Ingrid L, Lounes-Hadj Sahraoui A, Frederic L, Yolande D, Joel F. 2016. Arbuscular mycorrhizal wheat inoculation promotes alkane and polycyclic aromatic hydrocarbon biodegradation: microcosm experiment on aged-contaminated soil. Environ. Pollut. 213: 549-560.   DOI
69 Girkina NT, Turnerb BL, Ostlec N, Craigona J, Sjogerstena S. 2018a. Root exudate analogues accelerate $CO_2$ and $CH_4$ production in tropical peat. Soil Biol. Biochem. 117: 48-55.   DOI
70 Girkina NT, Turnerb BL, Ostlec N, Craigona J, Sjogerstena S. 2018b. Composition and concentration of root exudate analogues regulate greenhouse gas fluxes from tropical peat. Soil Biol. Biochem. 127: 280-285.   DOI
71 Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489: 220-230.   DOI
72 Florio A, Brefort C, Gervaix J, Berard A, Le Roux X. 2019. The responses of $NO_2{^-}$ and $N_2O$-reducing bacteria to maize inoculation by the PGPR Azospirillum lipoferum CRT1 depend on carbon availability and determine soil gross and net $N_2O$ production. Soil Biol. Biochem. 136: 107524.   DOI
73 Kim J, Yoo G, Kim D, Ding W, Kang H. 2017. Combined application of biochar and slow-release fertilizer reduces methane emission but enhances rice yield by different mechanisms. Appl. Soil Ecol. 117-118: 57-62.   DOI
74 Duan P, Zhang Q, Zhang X, Xiong Z. 2019. Mechanisms of mitigating nitrous oxide emissions from vegetable soil varied with manure, biochar and nitrification inhibitors. Agric. Forest Meteorol. 278: 107672.   DOI
75 Agamuthu P, Abioye OP, Aziz AA. 2010. Phytoremediation of soil contaminated with used lubricating oil using Jatropha curcas. J. Hazard. Mater. 179: 891-894.   DOI
76 Kao CM, Chen CY, Chen SC, Chien HY, Chen YL. 2008. Application of in situ biosparging to remediate a petroleum-hydrocarbon spill site: Field and microbial evaluation. Chemosphere 70: 1492-1499.   DOI
77 Ramadass K, Megharaj M, Venkateswarlu K, Naidu R. 2018. Bioavailability of weathered hydrocarbons in engine oil-contaminated soil: Impact of bioaugmentation mediated by Pseudomonas spp. on bioremediation. Sci. Total Environ. 636: 968-974.   DOI
78 Wang B, Xie HL, Ren HY, Li X, Chen L, Wu BC. 2019. Application of AHP, TOPSIS, and TFNs to plant selection for phytoremediation of petroleum-contaminated soils in shale gas and oil fields. J. Clean. Prod. 233: 13-22.   DOI
79 Limmer M, Burken J. 2016. Phytovolatilization of organic contaminants. Environ. Sci. Technol. 50: 6632-6643.   DOI
80 Barrutia O, Garbisu C, Epelde L, Sampedro MC, Goicolea MA, Becerril JM. 2011. Plant tolerance to diesel minimizes its impact on soil microbial characteristics during rhizoremediation of diesel-contaminated soils. Sci. Total Environ. 409: 4087-4093.   DOI
81 IPCC, 2013. In: Stocker, TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J, Nauels, A, Xia Y, Bex V, Midgley PM. (Eds.), Climate change 2013: The physical science basis. Contribution of working Ggoup I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK & New York, NY, USA.
82 Wright EL, Black CR, Turner B, Sjogersten S, 2013. Environmental controls of temporal and spatial variability in $CO_2$ and $CH_4$ fluxes in a neotropical peatland. Glob. Change Biol. 19: 3775-3789.   DOI
83 Cook RL, Hesterberg D. 2013. Comparison of trees and grasses for rhizoremediation of petroleum hydrocarbons. Int. J. Phytoremediat. 15: 844-860.   DOI
84 Lacalle RG, Gomez-Sagasti MT, Artetxe U, Garbisu C, Becerril JM. 2018. Brassica napus has a key role in the recovery of the health of soils contaminated with metals and diesel by rhizoremediation. Sci. Total Environ. 618: 347-356.   DOI
85 Kai T, Ikeura H, Ozawa S, Tamaki M. 2018. Effects of basal fertilizer and perlite amendment on growth of zinnia and its remediation capacity in oil-contaminated soils. Int. J. Phytoremediation 20: 1236-1242.   DOI
86 Liu R, Jadeja RN, Zhou Q, Liu Z. 2012. Treatment and remediation of petroleum-Contaminated soils using selective ornamental plants. Environ. Eng. Sci. 29: 494-501.   DOI
87 Brink SC. 2016. Unlocking the secrets of the rhizosphere. Trends Plant Sci. 21: 169-170.   DOI
88 Mhatrea PH, Karthikb C, Kadirvelu K, Divya KL, Venkatasalam EP, Srinivasan S, et al. 2019. Plant growth promoting rhizobacteria (PGPR): A potential alternative tool for nematodes bio-control. Biocatal. Agric. Biotechnol. 17: 119-128.   DOI
89 Gopalakrishnan S, Sathya A, Vijayabharathi R, Varshney RK, Gowda CLL, Krishnamurthy L. 2015. Plant growth promoting rhizobia: challenges and opportunities. 3Biotech 5: 355-377.
90 Cakmakci R, Donmez F, Aydm A, Sahin F. 2006. Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol. Biochem. 38: 1482-1487.   DOI
91 Siddiqui ZA, Mahmood I. 2001. Effects of rhizobacteria and root symbionts on the reproduction of Meloidogyne javanica and growth of chickpea. Bioresour. Technol. 79: 41-45.   DOI
92 Wang W, Neogi S, Lai DYF, Zeng C, Wang C, Zeng D. 2017. Effects of industrial and agricultural waste amendment on soil greenhouse gas production in a paddy field in Southeastern China. Atmos. Environ. 164: 239-249.   DOI
93 Hoyos-Santillan J, Lomax BH, Large D, Turner BL, Boom A, Lopez OR, et al. 2016. Quality not quantity: organic matter composition controls of $CO_2$ and $CH_4$ fluxes in neotropical peat profiles. Soil Biol. Biochem. 103: 86-96.   DOI
94 Yan F, Schubert S, Mengel K, 1996. Soil pH increase due to biological decarboxylation of organic anions. Soil Biol. Biochem. 28: 617-624.   DOI
95 Chen Y, Li S, Zhang Y, Li T, Ge H, Xia S, et al. 2019. Rice root morphological and physiological traits interaction with rhizosphere soil and its effect on methane emissions in paddy fields. Soil Biol. Biochem. 129: 191-200.   DOI