Introduction

Petroleum hydrocarbons are fossil fuels formed from organic matter; which are distributed in the subsoil layers and used for industrial energy production worldwide (Velásquez- Arias 2017). Currently, the presence of various kind of automobiles, the use of cleaning solvents, and some cosmetics may contain large amounts of hydrocarbons, which has caused an increase in their use (Ahmed and Fakhruddin 2018). The petroleum industry has grown in Colombia in recent years. The reserves of this fossil fuel are estimated to be about 1.5 billion barrels, which represents 26% of the country’s exports (Hernández-Rodríguez 2020). The growth of this industry has provided many benefits to the national economy by actively contributing to exports and the production of goods. The sector has further stimulated the generation of jobs and royalties for the financing of public expenditure (Hernández-Rodríguez 2020). However, unfortunately, petroleum sources also contribute to pollution and changes in land use as well as surface and groundwater utilization owing to exploitation, refining, lack of maintenance, and fuel theft (Sales da Silva et al. 2020). Moreover, Colombia has been affected by terrorist attacks approximately 829 times between 2007 and 2015 caused spills of thousands of barrels of hydrocarbons (Mendizabala et al. 2021). These problems may affect terrestrial and aquatic biodiversity due to landscape alteration (Sales da Silva et al. 2020).

In the abovementioned context, microorganisms with the potential to reduce pollutant levels by degradation processes have gained attention (Garzón et al. 2017; Sales da Silva et al. 2020). Bacteria are among those microorganisms that are able to convert the pollutants to less toxic molecules, and hence, allow the reclamation of large expanses of polluted areas (Hernández Ruiz et al. 2017; Renteria and Rosero 2019). Bacteria are capable of tolerating and using certain pollutants as sources of carbon and energy, contributing to the remediation of affected ecosystems (Marquez-Rocha et al. 2001). The oxygen-dependent enzymes called monooxygenases provide a means to use hydrocarbons as substrates, which allows the survival of bacteria in hydrocarbon-polluted environments (Das and Chandran 2011). Certain bacteria isolates such as Escherichia coli, Alcaligenes sp. and Thiobacter subterraneus can contribute in the degradation process by combining several metabolic pathways in a consortium to increase the extent of degradation of polycyclic aromatics hydrocarbons-PAHs (Pandey and Dubey 2012). Another important aspect is the presence of indigenous bacterial populations, which are of interest in degradation studies as they can be directly isolated from polluted sites and be characterized for a better understanding of the mechanism of biodegradation (Das and Chandran 2011).

The first study on bacterial degradation in Colombia, published in 1996, isolated bacteria belonging to the Pseudomonas genus from sediments highly polluted by PAHs (Vargas et al. 1996). Since then, several studies have been published, including reviews that list hydrocarbon-degrading bacteria (HDB) and discuss the importance of their management in polluted environments (Lozano 2005; Benavides-López et al. 2006; Trujillo-Toro and Ramírez-Quirama 2012; Garzón et al. 2017; De La Rosa Martinez and Rabelo-Florez 2020). However, thus far, there is no known review gathering data from all the research on hydrocarbon-degrading bacteria, advantages, and applications in Colombia. Since the problem of hydrocarbon pollution is of global relevance (Zhang and Chen 2017; Sales da Silva et al. 2020) and Colombia also considers it a critical issue. Therefore, in this review the objective is to identify all the studies on HDB conducted in the country so far. This paper provides an analysis about bacterial hydrocarbon degradation capability, pinpoint the areas in which degradation studies have been performed, and identify the most evaluated hydrocarbon. This information towards the better understanding in bioremediation challenges and will allow researchers interested in this field to have adequate baseline information to plan future studies.

Materials and methods

Investigations were selected from the Scielo, PubMed, Redalyc, ScienceDirect, Scopus, and Dialnet databases. Google Scholar was also used for the search of gray literature, and for peer reviewed articles. The following keywords were defined in Spanish (degradación, Colombia, hidrocarburos, bacterias), and in English (degradation, Colombia, hydrocarbon, bacteria). Different combinations of last keywords were employed to obtain a high number of publications in the exhaustive search. For the selection of publications suitable for analysis, the following inclusion criteria were established: type of study (original articles and theses), place (Colombia), degraded pollutant (petroleum, diesel, gasoline, motor oil), degrading microorganism (bacteria), publication date (between 1996 and 2021), and language (Spanish and English). During the literature search, those articles that did not meet the established criteria were excluded: articles about studies performed outside Colombia, degrading organisms other than bacteria, such as fungi, microalgae, and plants, and degraded pollutants other than hydrocarbons, such as heavy metals and pesticides.

The results of the analysis of the collected studies were recorded in a table using Microsoft® Excel 2019 according to author’s name, year of publication, source in which the study was conducted, type of study, and identified bacterium (genus and/or species). Additionally, an analysis to determine the behavior and the interest in studying HDB between 1996 and 2021 was performed. The impact and the interest in research on this topic in Colombia were assessed and compared with some reviews performed for other regions of the world.

Results

The exhaustive search yielded 1288 articles, 410 of which were published in Spanish and 878 in English (Table 1).

Table 1 General statistical information for the articles of hydrocarbon-degrading bacteria (until May 2021)
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After removal of the duplicate articles and application of the inclusion criteria, 37 articles were obtained (Fig. 1).

Fig. 1
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PRISMA flowchart showing the selection of the research articles of hydrocarbon-degrading bacteria in Colombia

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From the analysis of the 37 selected publications, it was observed that a high number of studies on bacterial hydrocarbon degradation were published mainly in 2018 (Fig. 2). This study was done in Colombia’s subnational territories, which comprise Bogotá as Capital District (C.D.), and 32 political-administrative entities called departments. Moreover, the country is divided into six natural regions constituted by differences in topography, weather, vegetation, types of soil and oil production. The Andean Region, covering the three branches of the Andes mountains; the Caribbean Region, covering the area adjacent to the Caribbean Sea; the Pacific Region adjacent to the Pacific Ocean; the Orinoquía Region, part of the Llanos plains mainly in the Orinoco River basin along the border with Venezuela; the Amazon Region, part of the Amazon rainforest; and finally the Insular Region, comprising islands in both the Atlantic and Pacific oceans (Fig. 3). Among the departments in which a high number of studies on HDB have been conducted are Antioquia and Cundinamarca with eight and seven publications respectively, located at Andean Region with a oil production of 319 Million barrels per day in 2020 (Minenergía 2021). Remarkably, the Orinoquía Region had the highest oil production, but two studies have been conducted only (Fig. 3).

Fig. 2
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Number of studies on HDB in Colombia between 1996 and 2020

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Fig. 3
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Map of Colombia showing the number of publications per department and oil production by region

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Pseudomonas sp. was the most representative genus of HDB on the papers in Colombia (Table 2). In the present study, 19 publications describing the isolation of bacteria belonging to this genus with Pseudomonas aeruginosa and Pseudomonas putida being the most frequently isolated species (Fig. 4). Furthermore, 7 publications reported bacteria belonging to the Bacillus genus (Table 2). Some studies did not report the bacterial genus and/or species because unidentified strains from bacterial consortia were used (Table 2). Among the analyzed studies, 16 on petroleum, 12 on diesel, 4 on gasoline, 1 on oil motor, 1 on kerosene, and 1 on tar. Three studies did not report the evaluated hydrocarbon (Table 2). In addition, an analysis of the universities, companies, and research groups that participated in the publications was performed (Table 3). The bacterial strains able to degrade hydrocarbons were isolated and identified, from soils samples mainly (Table 2).

Table 2 Studies of hydrocarbon degrading bacteria conducted in Colombia
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Fig. 4
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Hydrocarbon degrading bacteria (HDB) in Colombia and their frequency in the analyzed publications

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Table 3 Universities, companies, and research groups that have published on Hydrocarbon Degrading Bacteria (HDB) in Colombia
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Discussion

This systematic review was designed to provide the most complete, up-to-date list of studies about hydrocarbon-degrading bacteria (HDB) in Colombia, with a total of 37 investigations. Selecting the HDB is of profound significance in evaluating, developing, and designing strategies for bioremediation studies owing to their potential to adapt to polluted environments and convert the pollutants such as hydrocarbons to innocuous substances by degradation (Das and Chandran 2011). Moreover, it is important to perform studies to identify bacteria with degradation capability like an important step toward successful bioremediation (Reyes-Reyes et al. 2018). In the present review, we found that authors from different universities, companies, and research groups have conducted studies in Colombia to isolate HDB on environmental samples since 1996 (Vargas et al. 1996). For Colombia, 2003 was a year of substantial advances with regard to petroleum exploration given that reforms attracted foreign investment (Trujillo-Quintero et al. 2017). Probably, this is the reason for an increase in publications after 2003. Most of the publications were from 2018, it is likely that the above issue might have aroused the interest of different researchers to study microbial degradation and provide possible solutions for the pollution problem using bioremediation (Renteria and Rosero 2019). Moreover, the increasing available grants to investigations and doctoral formation in last year’s support the results obtained here (Minciencias 2019).

In the Andean Region, the departments of Antioquia and Cundinamarca, there are research groups in microbiology, chemical engineering, and biotechnology, among others. This observation emphasizes the fact that this region is very much interested in and at the cutting edge of studies in HDB. Concerning the research groups, the ones belonging to Universidad Nacional de Colombia, particularly in Medellín at Antioquia department, and Pontificia Universidad Javeriana in Bogotá, D.C. at Cundinamarca department reported the highest number of publications on HDB in Colombia. This establishes the need to continue the search for HDB in all the departments of the country, mainly in those located in regions with high oil production where can provide hydrocarbon residues.

The occurrence of some species belonging to the Pseudomonas and Bacillus genera and others mentioned here, constitutes valuable information for HDB present in Colombia. According to the analyzed publications, Pseudomonas and Bacillus species are the most frequently isolated in hydrocarbon degradation studies in the country. Probably, this result could be attributed to the much higher cultivability of both genera by direct isolation of contaminated samples with hydrocarbons (Gomez et al. 2006; Quintana-Saavedra et al. 2012; Álvares et al. 2016; Doria-Argumedo 2018). However, Pseudomonas and Bacillus are genera truly important and have been found to play vital roles in petroleum hydrocarbon degradation (Vásquez et al. 2010; Yanine 2010; Das and Chandran 2011; Xu et al. 2018). For example, P. aeruginosa has been identified as a HDB capable of degrading aromatic and polyaromatic hydrocarbons because it produces biosurfactants during its stationery growth phase, which facilitates the solubilization and therefore the degradation (Silva et al. 2018). Inoculation with P. aeruginosa bacteria had the highest rates of hydrocarbon removal, in ground contaminated samples with the Castilla`s crude, coming from 10 fields (Camargo-Millán and Acero-Pérez 2007). Pseudomonas putida is part of the soil microbiota and possesses enzymes called dioxygenases that are involved in hydrocarbon degradation (Truskewycz et al. 2019). On the other hand, species belonging to the Bacillus genus present high adaptability and can grow in extreme and hostile environments such as hydrocarbon contaminated soil and water (de Mesa et al. 2006; Valdivia-Anistro et al. 2018). Furthermore, the Bacillus genus is another bacterium reported as petroleum hydrocarbon degrader, and could be useful in reducing the levels of these hydrocarbons (Kolsal et al. 2017; Lima et al. 2020).

Another important result is taxonomic information for some HDB is unknown (Perdomo-Rojas and Pardo-Castro 2004; Vallejo et al. 2010; Yanine 2010; García et al. 2011). Additional investigations using molecular and other tools to identify all HDB is highly desirable in these cases. Overall, the taxonomy of environmental bacteria in Colombia is relatively poorly known. The taxonomic category of HDB is important for planning and interpreting future biodegradation studies (Ławniczak et al. 2020). In addition, the degradation of hydrocarbons is more effective when bacteria work together in a consortium. For example, Arrieta et al. showed the efficiency of a bacterial consortium that included the genera Arthrobacter, Bacillus, Flavobacterium, Sanguibacter, and Staphylococcus in the degradation of diesel (Arrieta-Ramírez et al. 2012). Vásquez et al. used a bacterial consortium composed of Acinetobacter, Bacillus brevis, Citrobacter, Enterobacter cloacae, Micrococcus, Nocardia, and Pseudomonas to study the degradation of oil sludge from a car wash (Vásquez et al. 2010). The hydrocarbons evaluated in the 37 selected publications; petroleum was the most studied one. In general, the authors suggest that short-chain aliphatic hydrocarbons such as those found in gasoline are more likely to volatilize and also tend to be toxic for bacteria (Suárez-Medellin and Vives 2004; Narváez-Flórez et al. 2008). This fact could explain why there are not as many studies on gasoline degradation as on petroleum.

This systematic review addresses studies specifically performed in Columbia with Columbian environmental samples. A more thorough investigation of knowledge about HDBs in different regions and their role in bioremediation of contaminated sites is useful. There are few similar studies that have systematically reviewed HDBs identified from specific regions or countries around the world. A review of remediation approaches for petroleum hydrocarbon contamination in the Arctic and Antarctic regions included bioremediation and identified bacteria isolated from these regions (Camenzuli and Freidman 2015). A recent review of PAH contamination in China, a country where rapid industrialization and urbanization have created fast economic growth, focused more on sources of PAHs in soils, but not on biodegradation (Zhang and Chen 2017). Other recent reviews examined more generally petroleum hydrocarbon biodegradation in aquifers (Logeshwaran et al. 2018) and provided an overview of enhanced hydrocarbon biodegradation strategies (Ławniczak et al. 2020). Notably, in Colombia a review article provided information regarding the most representative bacterium in biodegrading hydrocarbons Pseudomonas sp., Bacillus sp., Bacillus subtilis and Burkholderia sp. (De La Rosa Martinez and Rabelo-Florez 2020). A compilation of investigations conducted inside a specific country is important for establishing a baseline and needs for future research. This is especially pertinent in countries such as Colombia due to the presence of hydrocarbons as substantial contaminants in different ecosystems throughout the country, and where much research is still needed. We considering that it is also important that similar systematic reviews be conducted by researchers in the different countries to know the HDB and the studies that may be required to control hydrocarbons contamination.

Conclusions

A literature search yielded 1288 articles on HDB. After applying the inclusion criteria, 37 published studies were identified in Colombia between 1996 and 2020. However, among these, no doctoral theses were found. Most of the publications were from 2018, and Bacillus sp. and Pseudomonas sp. are the most studied genera in Colombia. Particularly, P. aeruginosa and P. putida are the most assessed species owing to the metabolic variation and enzymatic production that allow them to adapt to environments polluted with hydrocarbons. It was observed in several studies that hydrocarbon degradation is more efficient when bacterial consortia are used rather than pure cultures. The most studied hydrocarbon in Colombia is petroleum, while the least reported ones are oil motor, kerosene, and tar. Finally, this study is important because it provides useful information about bacteria that exhibit the potential to degrade hydrocarbons in Colombia.