SciELO - Scientific Electronic Library Online

vol.25 número1Germinación de dos variedades de Ochroma pyramidale (Cav. ex Lam.) Urb. de la Selva Lacandona, ChiapasRégimen hídrico e intercambio de gases de Prosopis laevigata (Humb. & Bonpl. ex Willd.) M. C. Johnst. en dos ecosistemas semiáridos del sur de Sonora índice de autoresíndice de assuntospesquisa de artigos
Home Pagelista alfabética de periódicos  

Serviços Personalizados




Links relacionados

  • Não possue artigos similaresSimilares em SciELO


Revista Chapingo serie ciencias forestales y del ambiente

versão On-line ISSN 2007-4018versão impressa ISSN 2007-3828

Rev. Chapingo ser. cienc. for. ambient vol.25 no.1 Chapingo Jan./Abr. 2019  Epub 15-Fev-2021 

Scientific article

Obtaining microorganisms in cloud forest soils for the degradation of aromatic hydrocarbons

Yair Cruz-Narváez1  * 

Enrique Rico-Arzate1 

José J. Castro-Arellano1 

Gerardo Noriega-Altamirano2 

Alberto Piña-Escobedo3 

Selvasankar Murugesan3 

Jaime García-Mena3 

1Instituto Politécnico Nacional-ESIQIE-UPALM, Laboratorio de Posgrado de Operaciones Unitarias. Edificio 7, Piso, Sección A, Av. Luis Enrique Erro s/n, Unidad Profesional Adolfo López Mateos, Zacatenco. C. P. 07738. Delegación Gustavo A. Madero, Ciudad de México, México.

2Universidad Autónoma Chapingo, Academia de Meteorología, Área de Agronomía. km 38.5 Carretera México-Texcoco. C. P. 56230. Chapingo, Texcoco, Estado de México, México.

3Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (Cinvestav), Departamento de Genética y Biología Molecular. Av. IPN 2508, col. Zacatenco. C. P. 07360. Gustavo A. Madero, Ciudad de México, México.



The impact of polluting substances, especially those of fossil fuels, on the environment is an important issue in the world. The ability of microorganisms to degrade these pollutants has been recently studied and characterized.


To analyze the ability of groups of microorganisms, obtained from a cloud forest ecosystem in Mexico, to degrade aromatic compounds (benzene, toluene, ethylbenzene and anthracene).

Materials and methods:

Microbiome samples were collected in the Sierra Madre del Sur in the state of Oaxaca. The microorganisms were isolated and identified by molecular techniques. Subsequently, the ability of the microorganisms to degrade aromatic hydrocarbons in a packed-bed bioreactor was quantitatively evaluated by HPLC-PDA chromatography.

Results and discussion:

Fifty groups of microorganisms were collected, cultured and genetically characterized. In genetic diversity, Lactobacillus, Prevotella and genera of the family Acetobacteraceae predominated. In the hydrocarbon biodegradation process, the pollutant concentration decreased 97 % and 91 % mineralization was achieved in less than 25 h.


The microorganisms showed significant degrading activity of the aromatic compounds. Biodiversity in the cloud forest in the Loxicha region is key to ensuring ecosystem services, so it is important to undertake explorations to evaluate the use of these bacterial microbiomes.

Keywords: Genetic characterization; soil pollutants; Lactobacillus; Prevotella; mineralization



El impacto de sustancias contaminantes en el ambiente es un tema importante en el mundo, especialmente el de los combustibles fósiles. La capacidad de los microrganismos para degradar estos contaminantes se ha estudiado y caracterizado recientemente.


Analizar la capacidad de grupos de microorganismos, obtenidos del ecosistema de bosque de niebla en México, para la degradación de compuestos aromáticos (benceno, tolueno, etilbenceno y antraceno).

Materiales y métodos:

Las muestras de microbiomas se recolectaron en la Sierra Madre del Sur en el estado de Oaxaca. Los microorganismos se aislaron e identificaron mediante técnicas moleculares. Posteriormente, la capacidad de los microorganismos para degradar hidrocarburos aromáticos, en un biorreactor de lecho empacado, se evaluó cuantitativamente mediante cromatografía HPLC-PDA.

Resultados y discusión:

Cincuenta grupos de microorganismos se recolectaron, cultivaron y caracterizaron genéticamente. En la diversidad genética predominaron Lactobacillus, Prevotella y géneros de la familia Acetobacteraceae. En el proceso de biodegradación de hidrocarburos, la concentración de contaminantes disminuyó 97 % y se produjo mineralización de 91 % en un tiempo menor de 25 h.


Los microorganismos mostraron importante actividad degradadora de los compuestos aromáticos. La biodiversidad en el bosque de niebla en la región Loxicha es clave para garantizar los servicios ecosistémicos, por ello, es importante emprender exploraciones para evaluar el uso de estos microbiomas bacterianos.

Palabras clave: Caracterización genética; contaminantes del suelo; Lactobacillus; Prevotella; mineralización


The microbial diversity present in ecosystems is a very important component and a determining factor of biological equilibrium (Ofek-Lalzar et al., 2014). The alteration undergone in an ecosystem has an impact on different scales and on physicochemical and biological parameters (Lareen, Burton, & Schäfer, 2016; Ofek-Lalzar et al., 2014). The characterization of microorganisms and their relative abundance in different environments provides very important information on both the preservation of this ecosystem and the potential use of native microorganisms (Panke-Buisse, Poole, Goodrich, Ley, & Kao-Kniffin, 2015).

In Mexico, climatic, orographic and water factors result in a wealth of environments. There are reports of isolation of different types of microorganisms from soils of various ecosystems in the country (Rodríguez-Zaragoza et al., 2008; Vásquez-Murrieta, Govaerts, & Dendooven, 2007). The main limitations for carrying out these processes have been the difficult access to the places to obtain samples and the multiple requirements for the isolation and identification of the microorganisms. Only 1 % of the microorganisms in a soil sample are cultivable in laboratory media (Ofek-Lalzar et al., 2014; Panke-Buisse, Lee, & Kao-Kniffin, 2017; Vaz-Moreira, Nunes, & Manaia, 2014); therefore, the application of a technique that does not require isolation and culture would allow the characterization of a larger fraction of the soil microbiology.

Soil should be conceived as a living entity, in which each of the microorganism groups function as organs of a biological entity, with specialized functions, but at the same time interconnected (Lareen et al., 2016; Nurulita, Adetutu, Gunawan, Zul, & Ball, 2016; Poosakkannu, Nissinen, & Kytöviita, 2017). Being a living organism, the soil can become diseased, and diagnosing the condition requires a series of specific analyses (Nurulita et al., 2016; Rota et al., 2013). The traditional approach is to characterize the physicochemical parameters of the soil to detect its deficiencies; however, the new paradigm is to evaluate it microbiologically and establish the degree of alteration of the processes that must occur naturally (Lareen et al., 2016; Panke-Buisse et al., 2017).

The impact of polluting substances on the environment has been studied for a long time; the most significant is that which occurs from fossil fuels. Since the Exxon Valdez oil spill in 1989, studies have been carried out on the ability of microorganisms to degrade this type of pollutant. The results have been favorable, thanks to the ability of microorganisms to adapt to the most severe conditions possible (Atlas & Bragg, 2009; Bacosa, Suto, & Inoue, 2011; Feng et al., 2007; Fukuyama, Shigenaka, & Coats, 2014; Rodriguez-R et al., 2015; Sharifi, Van Aken, & Boufadel, 2011). Because many fuel spills occur in soil and water, the option is to use microorganisms that adapt to these two conditions and that can pass from one medium to another while conserving their degrading ability, an intrinsic characteristic that only microorganisms are capable of developing (Boopathy, Shields, & Nunna, 2012; Bouchez-Naïtali & Vandecasteele, 2008; Guo et al., 2012; Patel, Cheturvedula, & Madamwar, 2012; Stepanyan & Voskoboinikov, 2006).

This study analyzed the ability of groups of microorganisms with stable symbiotic associations, obtained from a cloud forest ecosystem in Mexico, to degrade aromatic compounds (benzene, toluene, ethylbenzene and anthracene), the main pollutants present in fossil fuels. This type of forest is characterized by a mixed composition of temperate climate species in the canopy, tropical and subtropical ones in the sub-canopy and understory, and an abundance of mosses, epiphytes and tree ferns that confer ample biodiversity to this ecosystem; in addition, it is geologically associated with the Paleozoic Era. For this reason, the territory has a rich soil biology, which can be promising for the degradation of aromatic hydrocarbons.

Materials and methods

Vegetation sampling was carried out in the Sierra Madre del Sur in the state of Oaxaca, Pochutla district, at an elevation of 1 300 m, where there are archipelagos of the mesophilic mountain forest (Gual-Díaz & Rendón-Correa, 2014). After recording the number of trees, species abundance was calculated considering 10 sites located in different plots. To corroborate the data obtained, Margalef’s index was used for specific richness and Simpson’s for abundance. Margalef’s index is based on the relationship between the number of species (S) and the total number of individuals observed (N) and is defined as:

DMg=S-1lnN In turn, Simpson’s index is given by:


where, p i is the proportional abundance of species i; that is, the number of individuals of species i divided by the total number of individuals in the sample.

Obtaining groups of microorganisms

In the cloud forest archipelagos, 50 soil microbiome samples were collected in different areas of the ecosystem, as shown in Table 1. The methodology consisted of collecting soil, roots and leaves close to the trees, whose phenotypic characteristics are resistance and prosperity in inhospitable environments. Simple random sampling was carried out in sites with undisturbed vegetation, where the diversity of plants at the site and the amount of leaf litter on the ground were considered, starting from the hypothesis that the specimens of emerging trees should correspond to a biodiversity pattern in the soil.

The samples were cultured in a medium with a mixture of polysaccharides, in the facilities of the organic fertilizer and vermiculture production module at Autonomous Chapingo University’s San Ignacio Field. After the development of the microbiota in the culture systems, samples were taken for genetic identification.

Table 1 Location of soil microbiome samples in a cloud forest of the Sierra Madre del Sur in the state of Oaxaca, Mexico. 

Extraction region Microorganism groups Latitude Longitude
Region I F1-F10 16° 03´ 27.5´´ N 96° 37´ 08.7´´ W
Region II F11-F20 15° 59´ 06.2´´ N 96° 13´ 57.7´´ W
Region III F21-F30 15° 59´ 11.3´´ N 96° 42´ 2.8´´ W
Region IV F31-F40 16° 09´ 56.8´´ N 97° 29´ 45.1´´ W
Region V F41-F50 16° 01´ 00.2´´ N 96° 34´ 49.5´´ W

DNA Extraction and sequencing of amplicon libraries

Genetic material was extracted in accordance with the protocol indicated by the manufacturer of PowerSoil® (MO BIO Laboratories, Inc). The DNA was amplified by PCR (Polymerase Chain Reaction), using 50 μL of 1xPCR buffer (5mM KCl, 1mM Tris-HCl, pH 8.0), 2 mM MgCl2, 0.2 mM of each primer 16S rDNA with 1356 bp product), 0.2 mM dNTP, 0.05 U of recombinant Taq polymerase (Thermo scientific EP0402) and 10 ng of total nucleic acids. The PCR program was 25 cycles (30 s, 95 °C; 30 s, annealing temperature for primers; 30 s, 72 °C] in a GeneAmp PCR System 2700 thermocycler (Applied Biosystems, USA).

The amplified material was characterized by massive ion semiconductor sequencing (Ion Torrent equipment, USA) and the results were processed through a bioinformatic analysis to obtain the sequences and make the corresponding identification (García-Mena et al., 2016).

Packed bioreactor test

A continuous-flow borosilicate bioreactor was built, measuring 10 cm in diameter and 70 cm in length, in an isothermal configuration. The fixed bed was made from sterile, additive-free, pharmaceutical-grade cotton fiber. The continuous flow was maintained with a diaphragm dosing pump (Seko brand, USA), from 0 to 100 % flow, with capacity to allow a volumetric flow of 500 mL·min-1. The bioreactor feed culture was prepared in a 20-L glass container, sterile and with continuous aeration by means of a pump (ELITE brand, USA) with a capacity of 60 L·h-1 of air. The receptacle contained 20 L of minimum medium (1.2 mL·L-1 FeCl2 0.1 %, KH2PO4 0.5 g· L-1, MgCl2 0.4 g·L-1, NaCl 0.4 g·L-1, NH4Cl 0.4 g·L-1, CaCl2 0.05 g·L-1, 1mL·L-1 trace element solution [ZnSO4 10 mg·L-1, MnCl2 3.0 mg·L-1, H3BO4 30 mg·L-1, CoCl2 20 mg·L-1, CuCl2 1.0 mg·L-1, NiCl2 2.0 mg·L-1, Na2MoO4 3.0 mg·L-1]; all analytical-grade reagents were Fermont brand) enriched with glucose (2 g·L-1). This medium was inoculated with 2 mL of each of the 50 groups of microorganisms and developed up to the exponential growth phase, for five days at 30 °C. The microorganism count during the test in the feeding system was made with 3M brand Petrifilm plates for aerobes, according to the methodology indicated by the manufacturer. The pumping system was connected to the bioreactor with a flow of 50 mL·min-1, allowing the establishment and formation of a microbiological film at a temperature of 30 °C.

Once the biofilm was formed, the flow of the glucose-enriched medium was interrupted and the problem solution was fed, consisting of a mixture of the pollutants benzene, toluene, ethylbenzene and anthracene, with a concentration of 1 000 mg·L-1 each. The solution was fed to the bioreactor, taking samples every 5 h, to analyze the concentration of the pollutants present by HPLC-PDA. At the end of the experiment, the bioreactor packing was extracted and divided into equal parts with a length of 10 cm in order to study the behavior of the microorganisms along the system by means of characterization by genetic sequencing.

The mineralization achieved during the process was measured through the analysis of total organic carbon (TOC), inorganic carbon (IC) and total carbon (TC) in General Electric brand equipment (Innova model, USA) with a self-sampling device. The measurement conditions were 5 % sodium persulphate as oxidant and 15 % phosphoric acid. The pollutant mixture used during the test was determined in a HPLC system (Perkin Elmer brand, Flexar model, USA) with a Phenyl column 25 cm long by 4.6 mm in diameter, with particle size of 5 μm, in reverse phase, coupled to a PDA (photodiode array) detector. The working conditions were 95:5 acetonitrile:water and 1.0 mL·min-1 flow in isocratic regime. The preparation of the sample for injection into the chromatograph required a SPE (solid phase extraction) system, using 2-mL C18 cartridges, with a speed of 23 to 26 drops per minute. The cartridge was conditioned with 5 mL of HPLC-grade methanol, followed by loading of the sample, whose required volume ranged from 1 to 100 mL; subsequently, the cartridge was washed with 5 mL of distilled water, and elution of the components was carried out with 5 mL of HPLC-grade acetonitrile.

Results and discussion

Ninety-nine tree species used as shade trees in coffee plantations were counted, many of which are endemic; a total of 1 140 individuals were recorded. Predominant species included pines (Pinus spp.), oaks (Quercus spp.), sweetgum (Liquidambar spp.), magnolias (Magnolia spp.), caudillo (Oreomunnea mexicana [Standl.] J.-F. Leroy), Mexican hand tree (Chiranthodendron pentadactylon Larreat.) and tree ferns (Cyathea spp.). Margalef's diversity index was 13.92 and Simpson's was 0.96. The former indicates that the archipelagos of the mountain cloud forest in the Loxicha region are composed of a wide diversity of variable composition in number of species, and the fact the Simpson’s index is close to 1 ratifies that the site is diverse; the results reveal high biodiversity and abundance of each plant species. This was the criterion used in the selection of areas for microbial sampling and genetic sequencing of soil bacteria.

The sequencing results are shown in Figure 1. In all cases there are predominant genera, which vary in proportion. The different environmental conditions from which the microorganism groups were extracted allow the development of associations of this nature. Among the predominant genera in all samples are Lactobacillus, Prevotella and genera of the family Acetobacteraceae.

Figure 1 Variation of genera found in soil samples of the cloud forest ecosystem in the Sierra Madre del Sur in the state of Oaxaca. 

Figure 2 shows the disappearance rate of pollutants up to concentrations of the order of 10 mg·L-1 in a period of 10 h, which was stable until the end of the experiment (120 h). The growth of the microorganisms was of the order of 1 x 1017, with the maximum being 1.2 x 1018. Initially, there is a direct dependence between the presence of pollutants and the increase in the number of microorganisms. It is possible that the maintenance in the number of microorganisms, subsequent to the drastic decrease in the concentration of pollutants, is due to the formation of the biofilm, which has a favorable environment to sustain the viability of the microorganisms present in the system.

Figure 2 Disappearance rate of pollutants (B = benzene, T = toluene, E = ethylbenzene and A = anthracene) against microbial growth (MPN = Most Probable Number) in a packed-bed bioreactor.  

Biofilm formation implies that several extracytoplasmic proteins interact with the abiotic surface and osmolarity of the medium (O'Toole & Kolter, 1998). The medium and conditions in which the development of the biofilm was promoted, and the change in the substrate from glucose to the pollutant mixture, may have activated the signal for the maintenance of bacterial viability. This signal, product of the change in environmental stimulus, translates into the expression of a mutant transposon as reported in the literature (Monteiro et al., 2007; O'Toole & Kolter, 1998; Wu, Yeh, Lu, Lin, & Chang, 2008).

The bacterial physiology required for the degradation of pollutants follows multiple mechanisms, including the activation of the cytochrome P450 enzyme pathway, which catalyzes the biotransformation of xenobiotics, which is a crucial step in this metabolic process (Huang, Nemati, Hill, & Headley, 2012; Monteiro et al., 2007; Janikowski, Velicogna, Punt, & Daugulis, 2002).

The change undergone by microorganisms in the nutritional aspect is the first significant stimulus, where there is no glucose and predominant or total presence of polluting substrates. This change is evident in the production of extracellular polysaccharides to form the bacterial biofilm (Figure 3), which have a structural function and act as surfactant agents (Ławniczak, Kaczorek, & Olszanowski, 2011).

Figure 3 Development of the bacterial biofilm along the packed-bed bioreactor.  

Characterization of the biofilm by next generation sequencing shows the final behavior and establishment of communities and interactions along the length of the bioreactor. Figure 4 shows that the microbiological distribution had an important variation, despite maintaining constant temperature and oxygen saturation during the experiment, which are key factors in microbial aerobic metabolism. The distribution by sections in the bioreactor allowed establishing that the genera Bacteroides, Prevotella and Lactobacillus increased their presence up to 50 %.

Figure 4 Variation of genera found along the bioreactor during the biodegradation process of aromatic hydrocarbons.  

The degree of mineralization reached in the process is shown in Figure 5. The initial TOC corresponds to the amount of pollutants present in the solution. During the process, the IC increases due to the metabolic transformation that the microorganisms perform; however, at the end of the process, the sum of the TOC and the IC do not correspond to the initial TOC. The difference is the loss in the form of CO2, the waste product of the aerobic metabolism of microorganisms. During this process, the mineralization reached is 91 %. An additional stimulus such as the addition of a surfactant to the medium or a substrate favoring co-metabolism could increase the degree of mineralization.

Figure 5 Mineralization during the biodegradation process of aromatic hydrocarbons. Behavior of total organic carbon (OC), inorganic carbon (IC) and total carbon (TC).  


The biodiversity found in the cloud forest archipelagos in the Loxicha region is key to ensuring ecosystem services, so it is important to undertake explorations to evaluate the use of these bacterial microbiomes. The genetic diversity of the cloud forest ecosystem in the state of Oaxaca and the balance achieved are due to the proportion of microorganisms involved, with Lactobacillus, Prevotella and genera of the family Acetobacteraceae prevailing. These microorganisms showed degrading activity on aromatic compounds (benzene, toluene, ethylbenzene and anthracene) that constitute hydrocarbon fuels, until their mineralization.


The authors thank the following: Mexico’s National Science and Technology Council for supporting this study through the CONACyT-163235 INFR-2011-01 project; the National Polytechnic Institute (IPN) Higher School of Chemical Engineering and Extractive Industries; Autonomous Chapingo University and IPN’s Center for Research and Advanced Studies (Cinvestav) for allowing the work to be carried out in its facilities.


Atlas, R., & Bragg, J. (2009). Bioremediation of marine oil spills: when and when not - the Exxon Valdez experience. Microbial Biotechnology, 2(2), 213-221. doi: 10.1111/j.1751-7915.2008.00079.x [ Links ]

Bacosa, H. P., Suto, K., & Inoue, C. (2011). Preferential utilization of petroleum oil hydrocarbon components by microbial consortia reflects degradation pattern in aliphatic-aromatic hydrocarbon binary mixtures. World Journal of Microbiology and Biotechnology, 27(5), 1109-1117. doi: 10.1007/s11274-010-0557-6 [ Links ]

Boopathy, R., Shields, S., & Nunna, S. (2012). Biodegradation of crude oil from the BP oil spill in the marsh sediments of Southeast Louisiana, USA. Applied Biochemistry and Biotechnology, 167(6), 1560-1568. doi: 10.1007/s12010-012-9603-1 [ Links ]

Bouchez-Naïtali, M., & Vandecasteele, J.-P. (2008). Biosurfactants, an help in the biodegradation of hexadecane? The case of Rhodococcus and Pseudomonas strains. World Journal of Microbiology and Biotechnology, 24(9), 1901-1907. doi: 10.1007/s11274-008-9691-9 [ Links ]

Feng, L., Wang, W., Cheng, J., Ren, Y., Zhao, G., Gao, C., …Wang, L. (2007). Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proceedings of the National Academy of Sciences, 104(13), 5602-5607. doi: 10.1073/pnas.0609650104 [ Links ]

Fukuyama, A. K., Shigenaka, G., & Coats, D. A. (2014). Status of intertidal infaunal communities following the Exxon Valdez oil spill in Prince William Sound, Alaska. Marine Pollution Bulletin, 84(1-2), 56-69. doi: 10.1016/j.marpolbul.2014.05.043 [ Links ]

García-Mena, J., Murugesan, S., Pérez-Muñoz, A. A., García-Espitia, M., Maya, O., Jacinto-Montiel, M., …Núñez-Cardona, M. T. (2016). Airborne bacterial diversity from the low atmosphere of Greater Mexico City. Microbial Ecology, 72(1), 70-84. doi: 10.1007/s00248-016-0747-3 [ Links ]

Gual-Díaz, M., & Rendón-Correa, A. (2014). Bosques mesófilos de montaña en México: Diversidad, ecología y manejo. México: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Retrieved from ]

Guo, H., Yao, J., Cai, M., Qian, Y., Guo, Y., Richnow, H. H., … Ceccanti, B. (2012). Effects of petroleum contamination on soil microbial numbers, metabolic activity and urease activity. Chemosphere, 87(11), 1273-1280. doi: 10.1016/j.chemosphere.2012.01.034 [ Links ]

Huang, J., Nemati, M., Hill, G., & Headley, J. (2012). Batch and continuous biodegradation of three model naphthenic acids in a circulating packed-bed bioreactor. Journal of Hazardous Materials, 201-202, 132-140. doi: 10.1016/j.jhazmat.2011.11.052 [ Links ]

Lareen, A., Burton, F., & Schäfer, P. (2016). Plant root-microbe communication in shaping root microbiomes. Plant Molecular Biology, 90(6), 575-587. doi: 10.1007/s11103-015-0417-8 [ Links ]

Ławniczak, Ł., Kaczorek, E., & Olszanowski, A. (2011). The influence of cell immobilization by biofilm forming on the biodegradation capabilities of bacterial consortia. World Journal of Microbiology and Biotechnology, 27(5), 1183-1188. doi: 10.1007/s11274-010-0566-5 [ Links ]

Monteiro, S. A., Sassaki, G. L., de Souza, L. M., Meira, J. A., de Araújo, J. M., Mitchell, D. A., … Krieger, N. (2007). Molecular and structural characterization of the biosurfactant produced by Pseudomonas aeruginosa DAUPE 614. Chemistry and Physics of Lipids, 147(1), 1-13. doi: 10.1016/j.chemphyslip.2007.02.001 [ Links ]

Nurulita, Y., Adetutu, E. M., Gunawan, H., Zul, D., & Ball, A. S. (2016). Restoration of tropical peat soils: The application of soil microbiology for monitoring the success of the restoration process. Agriculture, Ecosystems & Environment, 216, 293-303. doi: 10.1016/j.agee.2015.09.031 [ Links ]

Ofek-Lalzar, M., Sela, N., Goldman-Voronov, M., Green, S. J., Hadar, Y., & Minz, D. (2014). Niche and host-associated functional signatures of the root surface microbiome. Nature Communications, 5, 4950. doi: 10.1038/ncomms5950 [ Links ]

O’Toole, G. A., & Kolter, R. (1998). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: A genetic analysis. Molecular Microbiology, 28(3), 449-461. doi: 10.1046/j.1365-2958.1998.00797.x [ Links ]

Panke-Buisse, K., Lee, S., & Kao-Kniffin, J. (2017). Cultivated sub-populations of soil microbiomes retain early flowering plant trait. Microbial Ecology, 73(2), 394-403. doi: 10.1007/s00248-016-0846-1 [ Links ]

Panke-Buisse, K., Poole, A. C., Goodrich, J. K., Ley, R. E., & Kao-Kniffin, J. (2015). Selection on soil microbiomes reveals reproducible impacts on plant function. The ISME Journal, 9(4), 980. doi: 10.1038/ismej.2014.196 [ Links ]

Patel, V., Cheturvedula, S., & Madamwar, D. (2012). Phenanthrene degradation by Pseudoxanthomonas sp. DMVP2 isolated from hydrocarbon contaminated sediment of Amlakhadi canal, Gujarat, India. Journal of Hazardous Materials, 201-202, 43-51. doi: 10.1016/j.jhazmat.2011.11.002 [ Links ]

Poosakkannu, A., Nissinen, R., & Kytöviita, M.-M. (2017). Native arbuscular mycorrhizal symbiosis alters foliar bacterial community composition. Mycorrhiza, 27(8), 801-810. doi: 10.1007/s00572-017-0796-6 [ Links ]

Rodriguez-R, L. M., Overholt, W. A., Hagan, C., Huettel, M., Kostka, J. E., & Konstantinidis, K. T. (2015). Microbial community successional patterns in beach sands impacted by the deepwater horizon oil spill. The ISME Journal, 9, 1928-1940. doi: 10.1038/ismej.2015.5 [ Links ]

Rodríguez-Zaragoza, S., González-Ruíz, T., González-Lozano, E., Lozada-Rojas, A., Mayzlish-Gati, E., & Steinberger, Y. (2008). Vertical distribution of microbial communities under the canopy of two legume bushes in the Tehuacán Desert, Mexico. European Journal of Soil Biology, 44(4), 373-380. doi: 10.1016/j.ejsobi.2008.05.003 [ Links ]

Rota, E., Caruso, T., Monaci, F., Baldantoni, D., De Nicola, F., Iovieno, P., & Bargagli, R. (2013). Effects of soil pollutants, biogeochemistry and microbiology on the distribution and composition of enchytraeid communities in urban and suburban holm oak stands. Environmental Pollution, 179, 268-276. doi: 10.1016/j.envpol.2013.04.026 [ Links ]

Sharifi, Y., Van Aken, B., & Boufadel, M. C. (2011). The effect of pore water chemistry on the biodegradation of the Exxon Valdez oil spill. Water Quality, Exposure and Health, 2(3-4), 157-168. doi: 10.1007/s12403-010-0033-4 [ Links ]

Stepanyan, O. V., & Voskoboinikov, G. M. (2006). Effect of oil and oil products on morphofunctional parameters of marine macrophytes. Russian Journal of Marine Biology, 32(S1), S32-S39. doi: 10.1134/S1063074006070042 [ Links ]

Janikowski, T., Velicogna, D., Punt, M., & Daugulis, A. (2002). Use of a two-phase partitioning bioreactor for degrading polycyclic aromatic hydrocarbons by a Sphingomonas sp. Applied Microbiology and Biotechnology, 59(2-3), 368-376. doi: 10.1007/s00253-002-1011-y [ Links ]

Vásquez-Murrieta, M. S., Govaerts, B., & Dendooven, L. (2007). Microbial biomass C measurements in soil of the central highlands of Mexico. Applied Soil Ecology, 35(2), 432-440. doi: 10.1016/j.apsoil.2006.06.005 [ Links ]

Vaz-Moreira, I., Nunes, O. C., & Manaia, C. M. (2014). Bacterial diversity and antibiotic resistance in water habitats: Searching the links with the human microbiome. FEMS Microbiology Reviews, 38(4), 761-778. doi: 10.1111/1574-6976.12062 [ Links ]

Wu, J.-Y., Yeh, K.-L., Lu, W.-B., Lin, C.-L., & Chang, J.-S. (2008). Rhamnolipid production with indigenous Pseudomonas aeruginosa EM1 isolated from oil-contaminated site. Bioresource Technology, 99(5), 1157-1164. doi: 10.1016/j.biortech.2007.02.026 [ Links ]

Received: June 27, 2018; Accepted: November 08, 2018

*Corresponding author:; tel.: 55 57 29 6000 ext. 54228.

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License