Publicado

2019-05-01

Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms

Impacto del petróleo crudo sobre grupos funcionales de bacterias cultivables y colonización de microorganismos simbióticos en la rizosfera de Clitoria-Brachiaria crecidas en mesocosmos

DOI:

https://doi.org/10.15446/abc.v24n2.64771

Palabras clave:

Arbuscular mycorrhizal fungi, crude oil, N-fixing free bacteria, P-solubilizing bacteria, root nodulation, soil contamination (en)
Bacterias fijadoras de N de vida libre, bacterias solubilizadoras de P, contaminación de suelo, hongos micorrízicos arbusculares, nodulación en raíz (es)

Autores/as

  • Alejandro Alarcón Colegio de Postgraduados
  • Mariano García Díaz Colegio de Postgraduados
  • Laura Verónica Hernández Cuevas Universidad Autónoma de Tlaxcala
  • Rosalba Esquivel Cote Colegio de Postgraduados
  • Ronald Ferrera-Cerrato Colegio de Postgraduados
  • Juan José Almaraz Suarez Colegio de Postgraduados
  • Ofelia Ferrera Rodriguez Instituto Nacional de Ecología A.C

This research evaluated the changes on populations of culturable N-fixing free bacteria (NFFB) and P-solubilizing bacteria (PSB), as well as on the root nodulation by native rhizobia, the root colonization and spore number of arbuscular mycorrhizal fungi (AMF), in the rhizosphere of Clitoria ternatea and Brachiaria brizantha grown in mesocosms contaminated with crude oil (0, 3000, 6000, 9000, and 12000 mg kg-1), for 240 days. After 24 h of soil contamination, the highest populations of NFFB and PSB (5.5 and 4.9 LogUFC, respectively) were found in control, and the lowest populations were obtained at 12000 mg kg-1 (5.1 and 4.2 LogUFC, respectively). In contrast, at 60 and 240 days, the control showed lower populations of NFFB and PSB (5.4 and 4.8 LogUFC, respectively) than contaminated treatments. The highest number or root nodules in C. ternatea was quantified in control at 60 and 240 days (25 and 27 nodules, respectively) in comparison to those observed at the treatment with 12000 mg kg-1 (7 and 1 nodule, respectively). At 60 days, AMF colonization in both plant species, and the number of spores significantly decreased as the crude oil concentration increased; however, at 240 days, the highest number of AMF spores was recorded at treatments with 6000 and 12000 mg kg-1. The dry weight of both plant species significantly decreased as crude oil concentrations increased. Although C. ternatea was more susceptible to the toxic effects of crude oil, this plant species showed greater content of total chlorophyll than B. brizantha.

Esta investigación evaluó los cambios en la población cultivable de bacterias de vida libre fijadoras de nitrógeno (BVLFN) y de bacterias solubilizadoras de fósforo (BSP), así como en la nodulación de raíces por rizobios nativos, y en la colonización y número de esporas de hongos micorrízicos arbusculares (HMA) en la rizósfera de Clitoria ternatea y Brachiaria brizantha cultivadas en mesocosmos contaminados con petróleo crudo (0, 3000, 6000, 9000 y 12000 mg kg-1), durante 240 días. A las 24 h de la contaminación del suelo, las poblaciones más altas de BVLFN y BSP (5,5 y 4,9 LogUFC, respectivamente) se encontraron en el control, mientras que las poblaciones más bajas se obtuvieron a 12000 mg kg-1 (5,1 y 4,2 LogUFC, respectivamente). En contraste, a los 60 y 240 días, el control mostró bajas poblaciones de BVLFN y BSP (5,4 y 4,8 LogUFC, respectivamente) que los tratamientos contaminados. El mayor número de nódulos en raíz de C. ternatea se cuantificó en el control a los 60 y 240 días (25 y 27 nódulos, respectivamente) en comparación con el tratamiento con 12000 mg kg-1 (7 y 1 nódulos, respectivamente). A los 60 días, la colonización de HMA en ambas especies vegetales y el número de esporas disminuyeron significativamente al aumentar la concentración de petróleo crudo; sin embargo, a los 240 días, se registró el mayor número de esporas de HMA en los tratamientos con 6000 y 12000 mg kg-1. El peso seco vegetal disminuyó significativamente al aumentar las concentraciones de petróleo crudo. Clitoria ternatea fue más susceptible a la toxicidad del petróleo, aunque esta especie vegetal mostró mayor contenido de clorofila total que B. brizantha.

Referencias

Adam G, Duncan H. The effect of diesel fuel on common vetch (Vicia sativa L.) plants. Environ Geochem Health. 2003;25(1):123-130. Doi: http://dx.doi.org/10.1023/A:1021228327540

Adenipekun CO, Oyetunji OJ, Kassim LS. Effect of spent engine oil on the growth parameters and chlorophyll content of Corchorus olitorius Linn. Environ. 2008;28(4):446-450. Doi: https://dx.doi.org/10.1007/s10669-008-9165-5

Akutam A, Pappoe ANM, Armah FA, Enu-Kwesi L. Phytoremediation potential of indigenous Ghanaian grass and grass-like species grown on used motor oil contaminated soils. J Ecol Environ. 2014;37(2):41-51. Doi: https://dx.doi.org/10.5141/ecoenv.2014.006

Alejandro-Córdova A, Rivera-Cruz MC, Hernández-Cuevas LV, Alarcón A, Trujillo-Narcía A, García-de la Cruz R. Responses of arbuscular mycorrhizal fungi and grass Leersia hexandra Swartz exposed to soil with crude oil. Water Air Soil Pollut. 2017;228(65):1-12. Doi: https://dx.doi.org/10.1007/s11270-017-3247-2

Alarcón A, Davies FT, Autenrieth, RL, Zuberer DA. Arbuscular mycorrhiza and petroleum-degrading microorganisms enhanced phytoremediation of petroleum-contaminated soil. Int J Phytorem. 2008;10(4):251-263. Doi: https://dx.doi.org/10.1080/15226510802096002

Alkorta I, Hernández-Allica J, Becerril JM, Amezaga I, Albizu I, Garbisu C. Recent findings on the phytoremediation of soils contaminated with environmentally toxic heavy metals and metalloids such as zinc, cadmium, lead, and arsenic. Rev Environ Sci BioTechnol. 2004;3(1):71-90. Doi: https://dx.doi.org/10.1023/B:RESB.0000040059.70899.3d

Barea JM. Biología de la rizosfera. Inv Ciencia. 1998;256:74-81.

Baruah P, Saikia RR, Baruah PP, Deka S. Effect of crude oil contamination on the chlorophyll content and morpho-anatomy of Cyperus brevifolius (Rottb.) Hassk. Environ Sci Pollut Res Int. 2014;21(21):12530-12538. Doi: https://dx.doi.org/10.1007/s11356-014-3195-y

Bento RA, Saggin-Júnior OJ, Pitard RM, Straliotto R, Ribeiro SEM, De Lucena-Tavares SR et al. Selection of leguminous trees associated with symbiont microorganisms for phytoremediation of petroleum-contaminated soil. Water Air Soil Pollut. 2012;223(9):5659-5671. Doi: https://dx.doi.org/10.1007/s11270-012-1305-3

Binet P, Portal JM, Leyval C. Application of GC±MS to the study of anthracene disappearance in the rhizosphere of ryegrass. Org Geochem. 2001;32(2):217-222. Doi: https://dx.doi.org/10.1016/S0146-6380(00)00168-6

Cabello MN. Hydrocarbon pollution: its effect on native arbuscular mycorrhizal fungi (AMF). FEMS Microbiol Ecol. 1997;22(3):233-236. Doi: https://dx.doi.org/10.1111/j.1574-6941.1997.tb00375.x

Cabello MN. Mycorrhizas and hydrocarbons. In: Fungi in Bioremediation, Gadd GM Editors. Surrey: British Mycological Society; 2001; p. 456-471.

Castillo C, Astroza I, Borie F, Rubio R. Efecto de cultivos hospederos y no hospederos sobre propágulos micorrízicos arbusculares. Rev Cienc Suelo Nutr Veg. 2008;8(1):37-54. Doi: https://dx.doi.org/10.4067/S0718-27912008000100004

Catriona MO, Macinnis-Ng P, Ralph J. In situ impact of petrochemicals on the photosynthesis of the seagrass Zostera capricorni. Mar Pollut Bull. 2003;46(11):1395-1407. Doi: https://dx.doi.org/10.1016/S0025-326X(03)00290-X

Châineau CH, Yepremian C, Vidalie JF, Ducreux J, Ballerini D. Bioremediation of a crude oil-polluted soil: biodegradation, leaching and toxicity assessments. Water Air Soil Poll. 2003;144(1):419-440. Doi: https://dx.doi.org/10.1023/A:1022935600698

Chibuike GU. Use of mycorrhiza in soil remediation: A review. Sci Res Essays. 2013;8(35):1679-1687. Doi: https://dx.doi.org/10.5897/SRE2013.5605

Chikere CB, Okpokwasili GC, Chikere BO. Bacterial diversity in a tropical crude oil-polluted soil undergoing bioremediation. African J Biotechnol. 2009;8(11):2535-2540.

Dai Y, Shen Z, Liu Y, Wanga L, Hannaway D, Lu H. Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. Environ Exp Bot. 2009;65(2-3):177-182. Doi: https://dx.doi.org/10.1016/j.envexpbot.2008.12.008

Dajoz R, Leiva-Morales MJ. Tratado de ecología. 2a ed. Madrid: Mundi Prensa; 2002. 600 p.

De Farias V, Maranho LT, Carvalho De Vasconcelos E, Da Silva Carvalho FA, Lacerda LG, Menegassi-Azevedo JÁ et al.. Phytodegradation potential of Erythrina crista-galli L., Fabaceae, in petroleum-contaminated soil. Appl Biochem Biotechnol. 2009; 157(1):10-22. Doi: https://dx.doi.org/10.1007/s12010-009-8531-1

De Ridder-Duine AS, Kowalchuk GA, Klein-Gunnewiek PJA, Gunnewiek K, Smant W, Van Veen JA et al. Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem. 2005;37(2):349-357. Doi: https://dx.doi.org/10.1016/j.soilbio.2004.08.005

Delille D, Pelletier E, Delille B, Coulon F. Effect of nutrients enrichment on the bacterial assemblage of Antarctic soils contaminated by diesel or crude oil. Polar Record. 2003;39(4):1-10. Doi: https://dx.doi.org/10.1017/S0032247402002863

Dellagnezze BM, Vasconcelos SG, Lopes ML, Ferreira DD, Limache EEG, Pantaroto VS et al. Bioremediation potential of microorganisms derived from petroleum reservoirs. Mar Pollut Bull. 2014;89(1-2):191-200. Doi: https://dx.doi.org/10.1016/j.marpolbul.2014.10.003

Dere S, Günes T, Sivaci R. Spectrophotometric determination of chlorophyll -a, b and total carotenoid contents of some algae species using different solvents. Tr J Bot. 1998;22:13-17.

Driai S, Verdin A, Laruelle F, Beddiar A, Sahraoui AL-H. Is the arbuscular mycorrhizal fungus Rhizophagus irregularis able to fulfil its life cycle in the presence of diesel pollution? Int Biodeter Biodegr. 2015;105:58-65. Doi: https://doi.org/10.1016/j.ibiod.2015.08.012

Essien J, Udoukpo F, Etesin U, Etuk H. Activities of hydrocarbon-utilizing and diazotrophic bacteria in crude oil impacted mangrove sediments of the Qua Iboe Estuary, Nigeria. Geosyst Engineer. 2013;16(2):165-174. Doi: http://dx.doi.org/10.1080/12269328.2013.805026

Ferrera-Cerrato R, Alarcón A. Rizosfera: Interacción suelo, planta y microorganismos. In: Ecología de la raíz, Fuentes-Dávila G, Ferrera-Cerrato R, editor(s). 2a ed. Ciudad Obregón: Sociedad Mexicana de Fitopatología, A.C.; 2007. p. 1-26.

Franco I, Contin M, Bragato G, De Nobili M. Microbiological resilience of soils contaminated with crude oil. Geoderma. 2004;121(1-2):17-30. Doi: https://dx.doi.org/10.1016/j.geoderma.2003.10.002

Franco-Ramírez A, Ferrera-Cerrato R, Varela-Fregoso L, Pérez-Moreno J, Alarcón A. Arbuscular mycorrhizal fungi in chronically petroleum contaminated soils in Mexico and the effects of petroleum hydrocarbons on spore germination. J Basic Microbiol. 2007;47(5):378-383. Doi: https://dx.dor.org/10.1002/jobm.200610293

García E, Ferrera-Cerrato R, Almaráz JJ, Rodríguez R, García E. Biodegradación de queroseno en la rizósfera de gramíneas en condiciones de invernadero. Agron Costarricense. 2013;37(2):125-134.

Gaspar ML, Cabello MN, Cazau MC, Pollero RJ. Effect of phenanthrene and Rhodotorula glutinis on arbuscular mycorrhizal fungus colonization of maize roots. Mycorrhiza. 2002; 12(2):55-59. Doi: https://dx.doi.org/10.1007/s00572-001-0147-4

Gerdemann JW, Nicolson TH. Spores of mycorrhizal endogone species extracted from soil by wet sieving and decanting. Trans Br Mycol Soc. 1963;46(2):235-244. Doi: https://dx.doi.org/10.1016/S0007-1536(63)80079-0

Gerdes B, Brinkmeyer R, Dieckmann G, Helmke E. Influence of crude oil on changes of bacterial communities in Arctic sea-ice. FEMS Microbiol Ecol. 2005;53(1):129-139. Doi: https://dx.doi.org/10.1016/j.femsec.2004.11.010

Harrier LA, Watson CA. The potential role of arbuscular mycorrhizal (AM) fungi in the bioprotection of plants against soilborne pathogens in organic and/or other sustainable farming systems. Pest Manage Sci. 2004;60(2):149-157. Doi: https://dx.doi.org/10.1002/ps.820

Hayat R, Ali S, Amara U, Khalid R, Ahmed I. Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol. 2010;60(4):579-598. Doi: https://dx.doi.org/10.1007/s13213-010-0117-1

Hernández-Ortega HA, Alarcón A, Ferrera-Cerrato R, Zavaleta-Mancera HA, López-Delgado HA, Mendoza-López MR. Arbuscular mycorrhizal fungi on growth, nutrient status, and total antioxidant activity of Melilotus albus during phytoremediation of a diesel-contaminated substrate. J Environ Manage. 2012;95:S319-324. Doi: https://dx.doi.org/10.1016/j.jenvman.2011.02.015

Hubalek T, Vosáhlová S, Matêju V, Kovácová N, Novotný C. Ecotoxicity monitoring of hydrocarbon-contaminated soil during bioremediation: a case study. Arch Environ Contam Toxicol. 2007;52(1):1-7. Doi: https://dx.doi.org/10.1007/s00244-006-0030-6

Jeffries P, Gianinazzi S, Perotto S, Turnau K, Barea J-M. The contribution of arbuscular mycorrhizal fungi in sustainable maintenance of plant health and soil fertility. Biol Fertil Soils. 2003;37(1):1-16. Doi: https://dx.doi.org/10.1007/s00374-002-0546-5

Joner EJ, Leyval C. Phytoremediation of organic pollutants using mycorrhizal plants: A new aspect of rhizosphere interactions. Agronomie 2003;23(5):495-502. Doi: https://dx.doi.org/10.1051/agro:2003021

Kaplan CW, Kitts CL. Bacterial succession in a petroleum land treatment unit. Appl Environ Microbiol. 2004;70(3):1777-1786. Doi: https://dx.doi.org/10.1128/AEM.70.3.1777-1786.2004

Kuo HC, Juang DF, Yang L, Kuo W-C, Wu Y-M. Phytoremediation of soil contaminated by heavy oil with plants colonized by mycorrhizal fungi. Int J Environ Sci Technol 2014;11(6):1661-1668. Doi: https://dx.doi.org/10.1007/s13762-013-0353-6

Labud V, Garcia C, Hernandez T. Effect of hydrocarbon pollution on the microbial properties of a sandy and a clay soil. Chemosphere 2007;66(10):1863-1871. Doi: https://dx.doi.org/10.1016/j.chemosphere.2006.08.021

Li G, Huang W, Lerner DN, Zhang X. Enrichment of degrading microbes and bioremediation of petrochemical contaminants in polluted soil. Water Res. 2000;34(15):3845-3853. Doi: https://dx.doi.org/10.1016/S0043-1354(00)00134-2

Linderman RG. Effects of mycorrhizas on plant diseases. In: Kapulnick Y, Douds DD editor(s). Arbuscular mycorrhizas: physiology and function. Amsterdam: Kluwer Academic Press; 2000. p. 345-366.

Lindström K, Jussila MM, Hintsa H, Kaksonen A, Mokelke L, Mäkeläinen K et al. Potential of the Galega-Rhizobium galegae system for bioremediation of oil-contaminated soil. Food Technol Biotechnol. 2003;41(1):11-16.

Liste HH, Felgentreu D. Crop growth, culturable bacteria and degradation of petrol hydrocarbons (PHCs) in a long-term contaminated field soil. Appl Soil Ecol. 2006;31(1-2):43-52. Doi: https://dx.doi.org/10.1016/j.apsoil.2005.04.006

Liu SL, Luo YM, Cao ZH, Wu LH, Ding KQ, Christie P. Degradation of benzo[a]pyrene in soil with arbuscular mycorrhizal alfalfa. Environ Geochem Health 2004;26(2):285-293. Doi: https://dx.doi.org/10.1023/B:EGAH.0000039592.80489.e5

Lorch HJ, Benckieser G, Ottow JCG. Basic methods for counting microorganisms in soil and water. In: Methods in applied soil microbiology and biochemistry, Alef K, Nannipieri P, editor(s). New York: Academic Press; 1995. p. 146-161.

Miranda-Martínez R, Delgadillo-Martínez J, Alarcón A, Ferrera-Cerrato R. Degradación de fenantreno por microorganismos en la rizosfera del pasto alemán. Terra Latinoamer. 2007;25(1):25-33.

Mitter B, Brader G, Afzal M, Compant S, Naveed M, Trognitz F et al. Chapter seven - Advances in elucidating beneficial interactions between plants, soil, and bacteria. Adv Agron. 2013;121:381-445. Doi: https://dx.doi.org/10.1016/B978-0-12-407685-3.00007-4

Morales-Guzmán G, Ferrera-Cerrato R, Rivera-Cruz MC, Torres-Bustillos LG, Arteaga-Garibay RI, Mendoza-López MR et al. A. Diesel degradation by emulsifying bacteria isolated from soils polluted with weathered petroleum hydrocarbons. Appl Soil Ecol. 2017;121:127-134. Doi: https://dx.doi.org/10.1016/j.apsoil.2017.10.003

Nageswara-Rao CV, Afzal M, Malallah G, Kurian M, Gulshan S. Hydrocarbon uptake by roots of Vicia faba (Fabaceae). Environ Monitor Assessment 2007;132(1-3):439-443. Doi: https://dx.doi.org/10.1007/s10661-006-9546-5

Naidoo G, Naidoo Y, Achar P. Responses of the mangroves Avicennia marina and Bruguiera gymnorrhiza to oil contamination. Flora. 2010;205(5):357-362. Doi: https://dx.doi.org/10.1016/j.flora.2009.12.033

Nie M, Wang Y, Yu J, Xiao M, Jiang L, Yang J et al. Understanding plant-microbe interactions for phytoremediation of petroleum polluted soil. Plos One 2011;6:e17961. Doi: https://dx.doi.org/10.1371/journal.pone.0017961

Njoku KL, Akinola MO, Oboh BO. Growth and performance of Glycine max L. (Merrill) grown in crude oil contaminated soil augmented with cow dung. Life Sci J. 2008;5(3):48-56.

Odjegba VJ, Sadiq AO. Effects of spent engine oil on the growth parameters, chlorophyll and protein levels of Amaranthus hybridus L. The Environ. 2002;22(1):23-28. Doi: https://dx.doi.org/10.1023/A:1014515924037

Osuji LC, Nwoye I. An appraisal of the impact of petroleum hydrocarbons on soil fertility: the Ozawa experience. Afr J Agric Res. 2007;2(7)318-324.

Phillips JM, Hayman DS. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc. 1970;55(1):158-161. Doi: https://dx.doi.org/10.1016/S0007-1536(70)80110-3

Pilon-Smits E. Phytoremediation. Annu. Rev Plant Biol. 2005;56:15-39. Doi: https://dx.doi.org/10.1146/annurev.arplant.56.032604.144214

Ramírez-Elías MA, Ferrera-Cerrato R, Alarcón A, Almaraz JJ, Ramírez-Valverde G, de-Bashan LE et al. Identification of culturable microbial functional groups isolated from the rhizosphere of four species of mangroves and their biotechnological potential. Appl Soil Ecol. 2014;82:1-10. Doi: https://dx.doi.org/10.1016/j.apsoil.2014.05.001

Rennie RJ. A single medium for the isolation of acetylene reducing (dinitrogen-fixing) bacteria from soils. Can J Microbiol. 1981;27(1):8-14. Doi: https://dx.doi.org/10.1139/m81-002

Rivera-Cruz MC, Trujillo-Narcia A, Miranda De La Cruz MA, Maldonado Chávez E. Evaluación toxicological de suelos contaminados con petróleos nuevo e intemperizado mediante ensayos con leguminosas. Interciencia. 2005;30(6):326-331.

Sangabriel W, Ferrera-Cerrato R, Trejo-Aguilar D, Mendoza-López MR, Cruz-Sánchez JS, López-Ortiz C et al. Tolerancia y capacidad de fitorremediación de combustóleo en el suelo por seis especies vegetales. Rev Int Contam Ambien. 2006;22(2):63-73.

Sanon A, Andrianjaka ZN, Prin Y, Bally R, Thioulouse J, Comte G et al. Rhizosphere microbiota interfers with plant-plant interactions. Plant Soil. 2009;321(1-2):259-278. Doi: https://dx.doi.org/10.1007/s11104-009-0010-5

SAS Institute Inc. The SAS system for windows, ver. 9.0. North Carolina: SAS Institute Inc.; 2002.

Singh DK. Biodegradation and bioremediation of pesticide in soil: concept, method and recent developments. Indian J Microbiol. 2008;48(1):35-40. Doi: https://doi.org/10.1007/s12088-008-0004-7

Spiares JD, Kenworthy KE, Rhykerd RL. Root and shoot biomass of plants seeded in crude oil contaminated soil. Texas J Agric Nat Res. 2001;14:117-124.

Stroud JL, Paton GI, Semple KT. Microbe-aliphatic hydrocarbon interactions in soil: implications for biodegradation and bioremediation. J Appl Microbiol. 2007;102:1239-1253. Doi: https://dx.doi.org/10.1111/j.1365-2672.2007.03401.x

Subba-Rao NS. Biofertilizers in Agriculture. New Delhi: Oxford and IBH Publishing; 1993. 208 p.

Sun W, Dong Y, Gao P, Fu M, Ta K, LI J. Microbial communities inhabiting oil-contaminated soils from two major oilfields in Northern China: implications for active petroleum-degrading capacity. J Microbiol. 2015;53(6):371-378. Doi: https://dx.doi.org/10.1007/s12275-015-5023-6

Tanee FBG, Akonye LA. Effectiveness of Vigna unguiculata as a phytoremediation plant in the remediation of crude oil polluted soil for Cassava (Manihot esculenta; Crantz) cultivation. J Appl Sci Environ Manag. 2009;13(1):43-47. Doi: https://dx.doi.org/10.4314/jasem.v13i1.55263

Tang M, Chen H, Huang JC, Tian ZQ. AM fungi effects on the growth and physiology of Zea mays seedlings under diesel stress. Soil Biol Biochem. 2009;41(5):936-940. Doi: https://doi.org/10.1016/j.soilbio.2008.11.007

Trujillo-Narcia A, Rivera-Cruz M, Lagunes-Espinoza LC, Palma-López DJ, Sánchez-Soto S, Ramírez-Valverde G. Uso de fertilizantes orgánicos en la enmendación de un fluvisol restaurado tras la contaminación con petróleo. Interciencia 2014;39(4):266-273.

Ullah A, Mushtaq H, Ali H, Munis MF, Javed MT, Chaudhary HJ. Diazotrophs-assisted phytoremediation of heavy metals: a novel approach. Environ Sci Pollut Res. 2015;22(4):2505-2514. Doi: https://dx.doi.org/10.1007/s11356-014-3699-5

Van Hamme JD, Singh A, Ward O. Recent advances in petroleum microbiology. Microbiol Molec Biol Rev. 2003;67(4):503-549. Doi: https://dx.doi.org/10.1128/MMBR.67.4.503-549.2003

Walker TS, Bais HP, Grotewold E, Vivanco JM. Root exudation and rhizosphere biology. Plant Physiol. 2003;132:44-51. Doi: https://dx.doi.org/10.1104/pp.102.019661

Wang W, Shi J, Xie Q, Jiang Y, Yu N, Wang E. Nutrient exchange and regulation in arbuscular mycorrhizal symbiosis. Molecular Plant. 2017;10(9):1147-1158. Doi: https://dx.doi.org/10.1016/j.molp.2017.07.012

Weidmann S, Sánchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V. Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant-Microbe Interact. 2004;17(12):1385-1393. Doi: https://dx.doi.org/10.1094/MPMI.2004.17.12.1385

Yan L, Penttinen P, Stoddard FL, Lindström K. Perennial crop growth in oil-contaminated soil in a boreal climate. Sci Total Environ. 2015;532:752-761. Doi: https://dx.doi.org/10.1016/j.scitotenv.2015.06.052

Yang S, Wen X, Zhao L, Shi Y, Jin H. Crude oil treatment leads to shift of bacterial communities in soils from the deep active layer and upper permafrost along the China-Russia crude oil pipeline route. PlosOne. 2014;9:e96552. Doi: https://dx.doi.org/10.1371/journal.pone.0096552

Zhang Q, Zhou Q, Ren L, Zhu YG, Sun SL. Ecological effects of crude oil residues on the functional diversity of soil microorganism in three weed rhizospheres. J Environ Sci. 2006;18(6):1101-1106. Doi: https://dx.doi.org/10.1016/S1001-0742(06)60046-6

Zhou G, Wang Y, Zhai S, Ge F, Liu ZH, Dai YJ et al. Biodegradation of the neonicotinoid insecticide thiamethoxam by the nitrogen-fixing and plant-growth-promoting rhizobacterium Ensifer adhaerens strain TMX-23. Appl Microbiol Biotechnol. 2013;97(9):4065-4074. Doi: https://dx.doi.org/10.1007/s00253-012-4638-3

Zhuang X, Chen J, Shim H, Bai Z. New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int. 2007;33(3):406-413. Doi: https://dx.doi.org/10.1016/j.envint.2006.12.005

Cómo citar

APA

Alarcón, A., García Díaz, M., Hernández Cuevas, L. V., Esquivel Cote, R., Ferrera-Cerrato, R., Almaraz Suarez, J. J. & Ferrera Rodriguez, O. (2019). Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms. Acta Biológica Colombiana, 24(2), 343–353. https://doi.org/10.15446/abc.v24n2.64771

ACM

[1]
Alarcón, A., García Díaz, M., Hernández Cuevas, L.V., Esquivel Cote, R., Ferrera-Cerrato, R., Almaraz Suarez, J.J. y Ferrera Rodriguez, O. 2019. Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms. Acta Biológica Colombiana. 24, 2 (may 2019), 343–353. DOI:https://doi.org/10.15446/abc.v24n2.64771.

ACS

(1)
Alarcón, A.; García Díaz, M.; Hernández Cuevas, L. V.; Esquivel Cote, R.; Ferrera-Cerrato, R.; Almaraz Suarez, J. J.; Ferrera Rodriguez, O. Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms. Acta biol. Colomb. 2019, 24, 343-353.

ABNT

ALARCÓN, A.; GARCÍA DÍAZ, M.; HERNÁNDEZ CUEVAS, L. V.; ESQUIVEL COTE, R.; FERRERA-CERRATO, R.; ALMARAZ SUAREZ, J. J.; FERRERA RODRIGUEZ, O. Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms. Acta Biológica Colombiana, [S. l.], v. 24, n. 2, p. 343–353, 2019. DOI: 10.15446/abc.v24n2.64771. Disponível em: https://revistas.unal.edu.co/index.php/actabiol/article/view/64771. Acesso em: 20 mar. 2026.

Chicago

Alarcón, Alejandro, Mariano García Díaz, Laura Verónica Hernández Cuevas, Rosalba Esquivel Cote, Ronald Ferrera-Cerrato, Juan José Almaraz Suarez, y Ofelia Ferrera Rodriguez. 2019. «Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms». Acta Biológica Colombiana 24 (2):343-53. https://doi.org/10.15446/abc.v24n2.64771.

Harvard

Alarcón, A., García Díaz, M., Hernández Cuevas, L. V., Esquivel Cote, R., Ferrera-Cerrato, R., Almaraz Suarez, J. J. y Ferrera Rodriguez, O. (2019) «Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms», Acta Biológica Colombiana, 24(2), pp. 343–353. doi: 10.15446/abc.v24n2.64771.

IEEE

[1]
A. Alarcón, «Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms», Acta biol. Colomb., vol. 24, n.º 2, pp. 343–353, may 2019.

MLA

Alarcón, A., M. García Díaz, L. V. Hernández Cuevas, R. Esquivel Cote, R. Ferrera-Cerrato, J. J. Almaraz Suarez, y O. Ferrera Rodriguez. «Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms». Acta Biológica Colombiana, vol. 24, n.º 2, mayo de 2019, pp. 343-5, doi:10.15446/abc.v24n2.64771.

Turabian

Alarcón, Alejandro, Mariano García Díaz, Laura Verónica Hernández Cuevas, Rosalba Esquivel Cote, Ronald Ferrera-Cerrato, Juan José Almaraz Suarez, y Ofelia Ferrera Rodriguez. «Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms». Acta Biológica Colombiana 24, no. 2 (mayo 1, 2019): 343–353. Accedido marzo 20, 2026. https://revistas.unal.edu.co/index.php/actabiol/article/view/64771.

Vancouver

1.
Alarcón A, García Díaz M, Hernández Cuevas LV, Esquivel Cote R, Ferrera-Cerrato R, Almaraz Suarez JJ, Ferrera Rodriguez O. Impact of Crude Oil on Functional Groups of Culturable Bacteria and Colonization of Symbiotic Microorganisms in the Clitoria-Brachiaria Rhizosphere Grown in Mesocosms. Acta biol. Colomb. [Internet]. 1 de mayo de 2019 [citado 20 de marzo de 2026];24(2):343-5. Disponible en: https://revistas.unal.edu.co/index.php/actabiol/article/view/64771

Descargar cita

CrossRef Cited-by

CrossRef citations10

1. Ibtissem Guergouri, Mounia Guergouri, Sabra Khouni, Yacine Benhizia. (2022). Identification of cultivable bacterial strains producing biosurfactants/bioemulsifiers isolated from an Algerian oil refinery. Archives of Microbiology, 204(10) https://doi.org/10.1007/s00203-022-03265-2.

2. Hadi Koohkan, Mohammad Seddiq Mortazavi, Ahmad Golchin, Fereshteh Saraji, Gholamali Akbarzadeh-Chomachaei. (2023). Comparison of Native Bacterial and Fungal Bioaugmentation in the Removal of Petroleum from Soil in the Presence of Sorghum. Water, Air, & Soil Pollution, 234(5) https://doi.org/10.1007/s11270-023-06298-5.

3. A. A. Farouq, H. Y. Ismail, A. B. Rabah, A. B. Muhammad, U. B. Ibrahim, A. Y. Fardami. (2022). Cowpea induced physicochemical and biological rhizosphere changes in hydrocarbon contaminated soil. Plant and Soil, 477(1-2), p.759. https://doi.org/10.1007/s11104-022-05460-y.

4. Ana Guadalupe Ramírez-May, María del Carmen Rivera-Cruz, María Remedios Mendoza-López, Rocío Guadalupe Acosta-Pech, Antonio Trujillo-Narcía, Consuelo Bautista-Muñoz. (2025). The Use of Rhizospheric Microorganisms of Crotalaria for the Determination of Toxicity and Phytoremediation to Certain Petroleum Compounds. Plants, 15(1), p.103. https://doi.org/10.3390/plants15010103.

5. Anushara Prabhakaran, Ramu Meenatchi, Surajit Pal, Saqib Hassan, Pallaval Veera Bramhachari, George Seghal Kiran, Joseph Selvin. (2022). Understanding the Microbiome Interactions in Agriculture and the Environment. , p.285. https://doi.org/10.1007/978-981-19-3696-8_15.

6. Fan Zhang, Guang Yang, Shuguang Wang. (2024). Effects of organic contaminants on arbuscular mycorrhiza formation: A meta-analysis. Applied Soil Ecology, 199, p.105425. https://doi.org/10.1016/j.apsoil.2024.105425.

7. Kaneez Fatima. (2019). Insights into Chemical Interaction between Plants and Microbes and its Potential Use in Soil Remediation. BioScientific Review, 01(04), p.39. https://doi.org/10.32350/BSR.0104.05.

8. Ana Carolina Guerrero-Chávez, Alejandro Alarcón, Ronald Ferrera-Cerrato, Irma Díaz-Aguilar, Ma. Remedios Mendoza-López, Bibiana Rios-Galicia, Ramón Ignacio Arteaga-Garibay, John Larsen. (2020). Diesel Impacts on Functional Bacterial Groups and Collembolans During Phytoremediation in a Mesocosm System. Water, Air, & Soil Pollution, 231(10) https://doi.org/10.1007/s11270-020-04854-x.

9. Débora M. de Souza, Jenifer de L. da Silva, Larissa da C. Ludwig, Brunna C. Petersen, Feliciane A. Brehm, Regina C. Espinosa Modolo, Tiago C. De Marchi, Rodrigo Figueiredo, Carlos A. M. Moraes. (2023). Study of the phytoremediation potential of native plant species identified in an area contaminated by volatile organic compounds: a systematic review. International Journal of Phytoremediation, 25(11), p.1524. https://doi.org/10.1080/15226514.2023.2170974.

10. José Alberto Orocio-Carrillo, María del Carmen Rivera-Cruz, Said Cadena-Villegas, Consuelo del Carmen Bautista-Muñoz, Antonio Juárez-Maldonado, Karla Chávez Álvarez. (2025). Composición química y adaptación del pasto tropical Leersia hexandra Sw. expuesto a suelo con petróleo crudo. Revista Mexicana de Ciencias Pecuarias, 16(1), p.81. https://doi.org/10.22319/rmcp.v16i1.6744.

Dimensions

PlumX

Visitas a la página del resumen del artículo

907

Descargas

Los datos de descargas todavía no están disponibles.