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Microbes and Petroleum Bioremediation

  • Bruna Martins Dellagnezze
  • Milene Barbosa Gomes
  • Valéria Maia de Oliveira
Chapter
  • 572 Downloads

Abstract

Petroleum pollution is an environmental issue often reported, including oil spills that occur accidentally worldwide. The release of large quantities of oil causes directly or indirectly huge environmental and economic impacts and may persist for decades. Bioremediation processes, such as biostimulation and bioaugmentation, among others, represent an eco-friendly and effective way to treat impacted areas based on the use of biological agents, associated or not to other compounds like biosurfactants in order to mineralize or complex organic and inorganic pollutant compounds. Therefore, this book chapter will review some topics related to bioremediation, including several in situ and ex situ techniques employed to treat polluted areas and the use of biosurfactants produced by several microorganisms. Moreover, oil spills and how they can affect marine and terrestrial environments are also mentioned, based on recent reports available in literature and according to organizations responsible for environmental impact monitoring. Hydrocarbonoclastic microorganisms have been described in both environments as well as the community dynamics of specific groups as a function of oil compounds input. In marine environments, a high abundance increase of a specific group called “obligate hydrocarbonoclastic bacteria (OHCB)” has been reported after an event involving petroleum contamination. Similar observation has been reported for mangroves, showing that oil or its derivatives allow the selection of microorganisms capable to degrade hydrocarbons. Petroleum contamination in cold environments, as Arctic and Antarctic regions, represents a huge challenge since management of contaminated sites and bioremediation effectiveness in these regions depend on several factors influencing oil degradation under cold conditions facing intrinsic limiting factors. In conclusion, bioremediation is not only a scientific concept described in literature but a concrete and applied efficient tool to treat polluted environments. The increasing number of bioremediation companies and patents also corroborates the tendency in search for new technologies and approaches focusing on sustainable management of polluted areas.

5.1 Introduction

Crude petroleum and its derivatives are still the main energy source for several countries and are among the most widely used substances in industrial processes. The world production of crude oil in 2015 was 41.4 million barrels per day (OPEC 2016). Activities related to petroleum industry as transport, extraction, refining, and distribution can affect directly or indirectly the surrounding ecosystems or even those in the transportation route. Due to the extensive application in several industrial sectors, petroleum hydrocarbons (PHCs) have been reported as a great pollutant source in the environment. Accidental oil spills, whether offshore or onshore, have been often reported and imply in major impact, affecting all the food web involved as well as human resources, mainly local communities economically dependent on natural resources for living.

Remediation techniques are already described and applied for contaminated environments, based mainly on physical treatment for the removal of contamination source. Instead, bioremediation is a technique employing microorganisms or their products to degrade or inactivate toxic compounds. Nevertheless, the success of this process is dependent on many biotic and abiotic factors.

Several microorganisms, as bacteria, fungi, and yeasts, whether from marine or terrestrial environments, are reported in literature as being capable to degrade diverse hydrocarbon compounds and/or used in bioremediation processes. In addition, some of them can produce biosurfactants, complex molecules which increase hydrocarbon degradation.

This book chapter will review some of the topics concerning bioremediation research. Contamination and fate of spilled petroleum in environment, as well as some of the microorganisms capable to degrade hydrocarbons, are described. In addition, some commercialized bioremediation products and how different bioremediation approaches have been investigated and applied for petroleum contamination as an eco-friendly and efficient tool for polluted environments are discussed.

5.2 Bioremediation

Anthropogenic activities have resulted in the dump of hazardous waste into the environment. These wastes represent pollutant sources of diverse types, such as pesticides, heavy metals, polyaromatic hydrocarbons (PAHs), polychlorinated biphenyls (PCB), antibiotics, dyes, and cleaning products (disinfectants and detergents), among others. Most of them are toxic to humans and animals, offering risks of diseases or even death (Verma and Jaiswal 2016). They can contaminate soil, surface water, groundwater, and air causing unpredictable environmental catastrophes. For this reason, remediation of contaminated environments has been an arduous task with countless researches aiming low cost-efficient solution.

In order to remove pollutants from contaminated sites, several physicochemical methods have been developed, such as solidification and stabilization, soil vapor extraction, soil washing, air sparging, thermal desorption, and incineration (Dadrasnia et al. 2013).

Such methods might be highly expensive and laborious, and, moreover, there is an inherent risk of worsening the situation by spreading pollutants (Salleh et al. 2003). Other common technologies used are evaporation, burying, dispersion, and washing (Das and Chandran 2011), but as a disadvantage, they often lead to incomplete decomposition. Then currently a simple and cost-effective method for hydrocarbon removal is necessary.

Bioremediation, although not a recent term, describes a natural process that uses biological agents (microorganisms or their products) in order to promote pollutant mineralization and recovery of the contaminated site. This approach presents lower costs and other advantages when compared to physicochemical processes (Table 5.1). According to the American Environmental Protection Agency (EPA), the definition of bioremediation consists in a “treatment that uses naturally occurring organisms to break down hazardous substances into less toxic or nontoxic substances.”
Table 5.1

Advantages and disadvantages of bioremediation techniques compared to conventional technology

Advantages

Disadvantages

Lower cost

May be difficult to control

Contaminants usually converted to innocuous products

Amendments introduced into the environment to enhance bioremediation may cause other contamination problems

Contaminants are destroyed, not simply transferred to different environments

May not reduce the concentration of contaminants to required levels

Persistent use

More time-consuming

According to literature, romans may have been the first ones to discover bioremediation during the development and establishment of biological treatment of wastewater and sewer. However, bioremediation process using microorganisms was invented by the American scientist George M. Robinson. He worked as an assistant petroleum engineer at Santa Maria & Company in California in the 1960s and devoted himself to experiments with a series of microbes in contaminated flasks (Sonawdekar 2012). The concept of commercial utilization gained acceptance throughout the 1960, but only in 1970 Dr. Chakrabarty described a crude oil-degrading bacterial strain of Pseudomonas putida, and 2 years later the first bioremediation commercial product was launched (Kundu et al. 2017). As consequence of Exxon Valdez oil spill event in 1989 in Alaska, the remediation using dispersants started to gain more visibility.

There are many different bioremediation techniques reported in literature using biological compounds (bacteria, fungi, plants) or enzymes. Although the techniques described can be applied to a diverse range of contaminants, hydrocarbons are the most reported class of pollutants due to their wide contamination in water and soils (Firmino et al. 2015). The main goal of this technique is to reduce or eliminate toxic substances from contaminated sites through different pathways such as degradation, assimilation, or transpiration in the atmosphere, yielding nontoxic final products such as inorganic molecules, water, carbon dioxide, and microbial biomass (Van Hamme et al. 2003).

Bioremediation techniques can be managed on-site (or in situ), treating the contaminated material at the impacted site and off-site (or ex situ), which removes the contaminated matrix to be treated in other location (Azubuike et al. 2016). Several factors as costs, site characteristics, and type and concentration of pollutants can determine if bioremediation should be carried out ex situ or in situ (Fig. 5.1). There are many types of bioremediation treatments such as application of specific fungi species (mycoremediation), plants (phytoremediation, rhizofiltration), and microorganisms in general and their subproducts or nutrients (bioaugmentation, biostimulation, biopiles, natural attenuation, and biosurfactants), among others (Banerjee et al. 2016; Marykensa 2011).
Fig. 5.1

Bioremediation techniques (in situ and ex situ). (Source: Juwarkar et al. 2014)

5.2.1 Methods of In Situ Bioremediation

5.2.1.1 Bioventing

It is an in situ technique used to degrade pollutants in subsurface soil through the action of autochthonous microorganisms. In this case, air/nutrients are injected into wells dug at the site of contamination above water level. The injection of air leads to oxygenation of the contaminated soil, stimulating autochthonous microorganisms and accelerating biodegradation of pollutants. This technique has been proved to be very effective in remediating petroleum-contaminated soil, also for aromatic compounds, known as recalcitrant in the environment. The use of this approach has been reported for soil contaminated with phenanthrene, which was almost totally removed from soil matrix after 7 months (Hohener and Ponsin 2014; Frutos et al. 2010).

5.2.1.2 Bioaugmentation

Bioaugmentation consists of adding specific indigenous or genetically engineered microorganisms to the contaminated site (soil or water). This technique can be employed when pollutants are very complex and native soil microorganisms are not capable of degrading them. The addition of microorganisms enhances the metabolic capability of indigenous microbial populations, thus increasing the extent of degradation. Moreover, a “consortium” (a pool of metabolically diverse microorganisms) can be used at the polluted site and act in synergism with indigenous microbiota to improve bioremediation. Also, genetically engineered microorganisms (GEM) have been strongly considered to be applied in bioremediation process. Joutey and co-workers (2013) described the degradative capacity of GEM and demonstrated the degradation of various pollutants, as hydrocarbons and some heavy metals, under controlled conditions. According to Dellagnezze et al. (2016), the application of bioaugmentation strategy using a consortium composed by metagenomic clones and a strain of Bacillus subtilis (CBMAI 707) contributed to increased aromatic compounds degradation of crude oil in mesocosm assay. However, the major obstacles for GEM application are still ecological and environmental concerns and regulatory constraints (Juwarkar et al. 2014; Menn et al. 2008).

5.2.1.3 Biosparging

Similarly to bioventing, biosparging also uses indigenous microorganisms to degrade the pollutants, however in a saturated zone, where the pores and rock fractures are filled with water. Using the same purpose in order to stimulate and enhance the microbial metabolic activity, nutrients and/or oxygen are injected into the saturated zone (Garima and Singh 2014). It is used to reduce the petroleum products often dissolved in groundwater or adsorbed to the soil below water level. However, this technique is more efficiently used for the removal of medium-weight petroleum products, like diesel, kerosene, etc. This process can also be a mix between anaerobic and aerobic metabolic processes. Kao et al. (2008) have described a (BTEX)-contaminated aquifer plume treated with biosparging and observed this metabolic variation, proven by some alterations in several parameters such as dissolved oxygen, redox potentials, nitrate, sulfate, total culturable heterotrophs, total anaerobes, and methanogenic microorganisms.

5.2.1.4 Biostimulation

In some cases, effective remediation is not achieved based solely on indigenous microbial populations grown under environmental conditions; thus some additional nutrient source is needed in order to stimulate microbial activity by optimizing the surrounding environment of the contaminated site. By addition of oxygen, or other electron acceptors, autochthonous microbiota is stimulated and may improve degradation rates. Stimulants are added into the subsurface through injection wells (Adams et al. 2015).

5.2.2 Methods of Ex Situ Bioremediation

5.2.2.1 Landfarming

Landfarming is a remediation technology implemented above ground for contaminated soils through biodegradation where the contaminated soil is hollow out, added by microorganisms and nutrients, and spread out on the ground surface or liner. The soil is regularly stirred for aeration and mixing of microorganisms, nutrients, and pollutants. Biodegradation efficacy can be enhanced by optimizing temperature and nutrients in the contaminated soil. Addition of co-substrates and anaerobic pretreatment of soil also enhances the degradation process. This technique has been successfully used for bioremediation of benzene, toluene, and xylene (BTX pollutants) (Sonawdekar 2012).

5.2.2.2 Composting

Composting is a controlled biological process, where aerobic and thermophilic conditions prevail for the microbial degradation of contaminated materials resulting in stable end products that can be safely disposed into environment. In general, composting is accomplished by autochthonous microorganisms and wastes are transformed into less complex materials with mass decrease. The contaminated soil is excavated and blended with organic substances, like wood, animal and vegetal wastes, etc. Aeration, temperature, and moisture are closely monitored to achieve higher degradative efficiency. The thermophilic composting has been used to reduce the concentration of toxic compounds and to treat sewage sludge, diesel-contaminated soil, brewing wastes, antibiotic fermentation waste, and waste from processing units (Khan and Anjaneyulu 2006).

5.2.2.3 Biopiles

Biopile is a technique that combines the use of two other techniques, landfarming and composting, where compost piles remain under well-aerated condition. It is more refined in comparison to the landfarming method and controls the spread of contamination by volatilization and leaching. This technique is used for treatment of surface contamination of spilled hydrocarbon pollutants, mainly petroleum products, allowing the growth of autochthonous microbiota, whether aerobic or anaerobic (Onweremadu 2014).

5.2.2.4 Bioreactors

Biodegradation of contaminants can be carried out in large bioreactors to treat both solid and liquid waste. The solids or liquids contaminants are subjected to bioremediation under controlled conditions in specifically designed bioreactors. Many parameters such as nutrient supply, temperature, aeration, moisture, and the contact between microorganisms and pollutants are maintained at optimal conditions. Hence the degradation is very rapid and efficient. However, running costs of bioreactors are very high (Azubuike et al. 2016).

5.2.3 Effect of Biosurfactants on Bioremediation

Biological alternative for the use of chemical surfactants are biosurfactants. Martins et al. (2009) define the term “biosurfactant” as a compound obtained from an organism that acts in interfaces and significantly reduces the surface tension. Since biosurfactants are surfactants, they are also amphiphilic compounds containing one hydrophobic and one hydrophilic moiety (Darvishi et al. 2011).

Biosurfactants production is the action response of microorganisms to the limited bioavailability of hydrophobic organic and hydrophilic compounds. Bacteria, yeast, and fungi have already been described as biosurfactant producers. Due to their biological origin, they present some advantages compared to chemical surfactants, like better biocompatibility and biodegradability, reduced toxicity, activity and stability at extreme conditions of temperature, pH, and salinity (Abdel-Mawgoud et al. 2010; Calvo et al. 2009).

Biosurfactants can be characterized based on their physicochemical properties, microbial origin, and chemical composition (Pacwa-Plociniczak et al. 2011). According to their molecular weight, two groups can be defined. The first group consists of low-molecular-weight compounds such as lipopeptides, glycolipids, and phospholipids. These molecules can act in surface and interfacial tension, increasing the surface area of insoluble organic compounds. Also, they can encapsulate hydrophobic compounds in the surfactant micelle core, resulting in an increase of the availability of hydrophobic compounds for microorganisms capable to degrade such compounds (Banat et al. 2010). The second group consists of high-molecular-weight compounds such as polysaccharides, proteins, lipopolysaccharides, lipoproteins, and biopolymers. High-molecular-weight bioemulsifiers promote the stabilization of emulsion formed by hydrocarbons and water, increasing the surface area for biodegradation (Banat et al. 2010; Darvishi et al. 2011).

However, glycolipids are the only microbial surfactants fully commercialized as a mixture for bioremediation purposes, and rhamnolipids, trehalolipids, and sophorolipids are among the most well-known and intensively studied low-molecular-weight biosurfactants (Shekhar et al. 2015; Franzetti et al. 2010).

5.2.4 Recent Strategies for Bioremediation

Adams et al. (2015), in a recent review, described techniques that are gaining visibility using GEM capable to degrade specific contaminants. These techniques were firstly reported in the late 1980s and early 1990s, but due to the widespread use and rapid development of molecular tools, they have gained prominence. Engineering microorganisms aiming degradative properties is based on several possibilities to explore and discover new metabolic and genetic diversity of microorganisms (Fulekar 2009).

Microbial electrochemical technologies (MET), a recent bioremediation strategy, consist in anaerobic systems where microorganisms can act through electrodes that can be placed in the contaminated area (Palma et al. 2017). In addition, nanoparticles have been used for bioremediation purposes. They can act increasing the bioavailability of hydrophobic components (Rizwan et al. 2014). Further, nanoparticles can also be used to immobilize bacterial cells that are capable of degrading specific toxic compounds or to biorecover certain compounds (Kumar et al. 2016; Shan et al. 2005).

5.2.5 Microbial Bioremediation of Hydrocarbons

Degradation of vast hydrophobic compounds by microorganisms has contributed to the application of bioremediation as a biotechnological process. The use of microorganisms has been considered an important tool, since it can promote the complete removal of pollutants from different contaminated environments (Demnerova et al. 2005). The capability for organic pollutant degradation is reported occurring in many species whether through aerobic or anaerobic process, leading to the modification of complex and recalcitrant lipophilic organic molecules into simple water-soluble products. However, the degradation of a broad range of compounds cannot be achieved by only one single bacterium. In order to potentialize the degradation of complex compounds, the use of a microbial association or consortium is more suitable in which the combination of diverse genetic background can provide a more efficient process (Joutey et al. 2013). They attack the organic chemicals by their enzymatic apparatus after getting into contact with specific or structurally related compounds which induce or depress the microbial enzymatic activity. This process occurs by a successive chain of reactions that usually involves a microbial consortium and their ecological interactions (synergism and co-metabolism).

According to Chikere et al. (2011), there are 81 genera of microorganisms described as being able to carry out biodegradation of petroleum or its derivatives in different environments. These microorganisms include members of the phyla Proteobacteria (Achromobacter, Acinetobacter, Alcaligenes, Sphingomonas, Pseudomonas), Actinobacteria (Arthrobacter, Corynebacterium, Dietzia), Firmicutes (Bacillus), and Bacteroidetes (Flavobacterium), unculturable bacterial clones, and members of the fungal phyla Ascomycota (Aspergillus, Penicillium), Zygomycota (Cunninghamella), subphylum Mucoromycotina (Mucor), and Basidiomycota (Phanerochaete, Sporobolomyces), among others.

The degradation ability of natural microbial communities from different habitats makes their catabolic potential even more versatile to transform organic compounds into inert and nontoxic molecules (Banerjee et al. 2016).

5.3 Oil Spills and Contamination

Petroleum is composed by a blend of hydrocarbons and can contain dozens of thousands of organic compounds chemically diverse, including some heavy metals. Petroleum chemical and physical properties may vary according to some features from reservoirs as age, location, and depth (Van Hamme et al. 2003; Head et al. 2003). The general classification of crude oil is resumed to light, medium, or heavy oil. This specification is based on their composition (proportions of the high-molecular-weight compounds) and products generated from their respective distillation process such as paraffins, naphthenes, or aromatic compounds. Light oils contain more saturated and aromatic hydrocarbons and a small proportion of resins and asphaltenes. On the other hand, the largest fraction of heavy oils consists of polar compounds, whereas saturated and aromatic hydrocarbons are in lower proportion (Head et al. 2003).

In accordance with Van Hamme and collaborators (2003), the biodegradability level of the oil components is dependent on their structure, meaning the more structurally complex the molecule, the more complex is its degradation process. Generally, biodegradation starts from structurally simpler molecules as n-alkanes and moves forward to compounds of higher structural complexity such as branched-chain alkanes and low molecular-weight n-alkyl aromatics, until more complex molecular structures as monoaromatics, cyclic alkanes, polycyclic aromatic hydrocarbons (PAHs), and asphaltenes.

Biodegradation of crude oil leads to changes in its composition. However, in general, biodegraded oils present high quantity of polar compounds which are more complex molecules and, in turn, more resilient to degradation than saturated and aromatic hydrocarbons. Moreover, heavier fractions of petroleum are more toxic and persistent and when released in the environment can cause long-term impact (Hassanshahian and Cappello 2013).

5.3.1 Oil Spills in Marine Environments

Energy use from oil sources has increased after World War II, in which the demand for economic development is directed toward oil exploration and exploitation which, inevitably, were accompanied by oil spills. Marine oil spills have become a category of anthropogenic disasters that seriously affect humans in several ways as ecologically and economically, besides the long-term damages to marine ecosystem (Mei and Yin 2009).

The most frequently described accidental oil spills occur offshore, where the marine contamination is broadly reported (Vieites et al. 2004; Doval et al. 2006; Wieczorek et al. 2007; Outdot and Chaillan 2010; Hazen et al. 2010). Hassanshahian and Cappello (2013) reported an estimate on the general causes of oil spills in which almost 50% come from natural seeps and less than 9% from catastrophic releases. However, 40% of marine oil input is related to consumption and urban discharge.

The release of large quantities of oil impacts directly or indirectly marine environments, affecting all food web, from phytoplankton to large mammals (Perelo 2010; Peterson et al. 2003). These damages can occur immediately and persist for decades. Besides affecting the environment, oil spills have major impacts on economy and human resources, mainly for communities that depend on marine resources, as fishermen. In 2012, a comparative study involving two cases of massive oils spills (Exxon Valdez and Deepwater horizon) assessed the mental health of affected people. Researchers observed high stress levels and also depression associated to economic losses from affected natural resources (gill et al. 2012).

The last update report developed by ITOPF (the International Tanker Owners Pollution Federation) published in February 2017 describes the major spillages from tankers since 1970 (Table 5.2). Main reasons of oils spills are related to structural damages, collision, grounding, fires, and explosions. Spills are characterized by the type of oil spill and the cause and location of accident. Moreover, spills are categorized by size (amount): (1) higher than 7 tonnes, (2) between 7 and 700 tonnes, and (3) higher than 700 tonnes.
Table 5.2

Major accidents involving oil spills from tankers since 1967. Source: Oil Tanker Spill Statistics, 2017 (ITOPF)

Position

Ship name

Year

Location

Spill size (tonnes)

1

Atlantic Empress

1979

Off Tobago, West Indies

287.000

2

ABT Summer

1991

700 nautical miles from Angola

260,000

3

Castillo de Bellver

1983

Off Saldanha Bay, South Africa

252,000

4

Amoco Cadiz

1978

Off Britany, France

223,000

5

Haven

1991

Genoa, Italy

144,000

6

Odyssey

1988

700 nautical miles of Nova Scotia, Canada

132,000

7

Torrey Canyon

1987

Scilly Isles

119,000

8

Sea Star

1972

Gulf of Oman

115,000

9

Irene Serenade

1980

Navarino Bay, Greece

100,000

10

Urquiola

1976

La Coruna, Spain

100,000

11

Hawaiian Patriot

1977

300 nautical miles off Honolulu

95,000

12

Independenta

1979

Bosphorus, Turkey

95,000

13

Jakob Maersk

1978

Oporto, Portugal

88,000

14

Braer

1993

Shetland Island, UK

85,000

15

Aegean Sea

1992

La Coruna, Spain

74,000

16

Sea Empress

1996

Milford Haven, UK

72,000

17

Mark V

1989

120 nautical miles off Morocco

70,000

18

Nova

1985

Off Kharg Island, Gulf of Iran

70,000

19

Katina P

1992

Off Maputo, Mozambique

67,000

20

Prestige

2002

Off Galicia, Spain

63,000

21

Exxon Valdez

1989

Prince William Sound, Alaska, USA

37,000

22

Hebei Spirit

2007

South Korea

11,000

The case of petroleum tanker Exxon Valdez at Alaska coast, in 1989, had a large and long-term impact, releasing about 40 million liters that spread more than 1300 km in the shoreline of the Gulf of Alaska. The application of commercial fertilizers as biostimulation approach was done throughout the coast, with 2237 fertilizer applications along the shoreline. After 3 years of the accident, most part of oil had been removed and the cleanup process was concluded (atlas and Hazen 2011). However, years after the accident, in a toxicological research, authors still observed abnormalities in algae populations, invertebrates, some species of birds, and mammals that were exposed to chronic pollution, even in significantly less (sublethal) quantity (Peterson et al. 2003).

A more recent case involving the oil company British Petroleum (BP) occurred in 2010, in Mississippi, when oil and gas with high pressure escaped from BP’s Deepwater Horizon well with subsequent explosion causing 11 deaths. The oil flowed out from the well for a period of 84 days, releasing about five million barrels spread along 690 miles of US coastline. Several measures were taken to retain the oil, as follows: 3% of oil were skimmed (skimmers are collector vessels containing devices where the superficial layer of the oil is drawn), 5% were burned (burning of oil is a strategy used in a controlled area in order to clear areas in a short time), 8% were chemically dispersed (approximately 1.4 million gallons of dispersants were used), 16% underwent natural dispersion, 17% were captured, 25% underwent evaporation or were dissolved, and 26% were remnant (Chen and Denison 2011; Atlas and Hazen 2011). In this case, biostimulation was not a feasible strategy, since the large amount of oil added of a great amount of nutrients or oxygen could lead to eutrophication. Nonetheless, several works have mentioned a shift in marine microbial communities, with significant increase in microbial groups capable of degrading hydrocarbon molecules, observed during or after petroleum leakage (Hazen et al. 2010; Kostka et al. 2011).

5.3.2 Fate of Oil in the Sea

When an oil spill occurs in the marine environment, petroleum derivatives can undergo several physicochemical and biological processes, called weathering. Physicochemical processes include evaporation, dissolution, dispersion, emulsification, photooxidation, adsorption sinking, and sedimentation. Biological weathering consists in biodegradation through microorganisms and ingestion by other organisms (Hassanshahian and Cappello 2013).

Moreover, in case of oil spill, many factors, as temperature, wind, and sea conditions, can determine the fate of oil in the sea and the contamination of ecosystems (Fig. 5.2).
Fig. 5.2

Fate of oil in seawater by different pathways. (Source: Chen and Denison (2011))

As consequence of spill, oil spreads on the surface forming a slick layer and interfering in nutrient and light penetration in water column, with negative impact on the photosynthesis process from phytoplankton (Carrera-Martínez et al. 2010; González et al. 2009). Volatile compounds and petroleum light fraction evaporate more rapidly, also depending on the type of oil and environmental parameters. Other fraction can adhere to suspended solids in the water column and contaminate deep sediment layers.

Sunlight-dependent photooxidation reactions (photolysis) also can occur, being restricted by the privation of sunlight. However, products from photooxidation process, such as toxic acids and phenolic compounds, are normally diluted into the vast volumes of seawater and thus do not cause harmful toxic effects (Kingston 2002). Hydrocarbon dissolution can occur mainly for low-molecular-weight molecules (less than 1%), which in turn can be easily degraded. Dispersion is possibly the main process responsible for natural removal of the majority of petroleum pollution on surfaces. As consequence, oil is “partitioned” in droplets and mixed to the water column, thus becoming more easily accessed for bacterial degradation (Chen and Denilson 2011).

Under specific conditions, oil-water emulsion can be formed. This process happens when water droplets are mixed to the oil layer on the surface, forming a viscous substance called “mousse”; its stability and formation are also dependent on the type of spilled oil. Mousse formation can determine the persistence of oil layer on the ocean surface (Kingston 2002).

Biological recovery of an ecosystem affected by oil spill is related to toxicity level as well as other elements that cause risks to normal biological functions. Thus, the recovery of an impacted environment can start from the decline of toxic compounds until a tolerable level for most of organisms and will depend on several abiotic and biotic factors, such as time of year, availability of colonizing microorganisms, and biological and climate interactions, among others (Kingston 2002; Chen and Denison 2011).

5.3.3 Marine Hydrocarbon Degrading Bacteria

Marine bacterial communities have been studied in order to identify possible microbial degraders and their metabolic potential. Thus, studies regarding the discovery and identification of key organisms capable to degrade contaminants are highly relevant, especially for the development of new in situ bioremediation strategies (Hassanshahian and Cappello 2013).

There are some typical microbial patterns after an event involving petroleum contamination, with large increase in abundance of some groups, such as Alcanivorax spp., reported as alkane degrader; Cycloclasticus spp., which degrade PAHs; Marinobacter and Thalassolituus, also present in temperate environments; and Oleispira, an obligate alkane-degrading psychrophile present in cold marine environments. Some marine degraders are highly specialized obligate hydrocarbon utilizers, called marine “obligate hydrocarbonoclastic bacteria (OHCB)” (Table 5.3). Approximately 90% of the microbial community present when an oil spill occurs consist of obligate hydrocarbon-degrading bacteria, which play a significant role in the natural remediation of oil-polluted marine environment (Yakimov et al. 2007; McGenity et al. 2012).
Table 5.3

Main bacterial genera belonging to the OHCB (obligate hydrocarbonoclastic bacteria) group

Bacterial genus

Substance

References

Alcanivorax

Crude oil

Yakimov et al. (1998), Kotska et al. (2011), and Santisi et al. (2015)

Cycloclasticus

Crude oil/ PAH

Kasai et al. (2002), Maruyama et al. (2003), and Kimes et al. (2014)

Marinobacter

Crude oil/ phenanthrene

Jurelevicius et al. (2013), Fathepure (2014), and Gomes et al. (2018)

Oleispira

Crude oil

Yakimov et al. (2007) and Brooijmans et al. (2009)

Thalassolituus

Crude oil

Yakimov et al. (2007), McKew et al. (2007), Dong et al. (2014), and Sanni et al. (2015)

The OHCB are widely distributed; however some species belonging to this group have only been detected in cold waters (e.g., Oleispira antarctica). Also, it has been reported that the type of hydrocarbon contamination can select specific genera, such as aliphatics degrading Alcanivorax and aromatic compounds degrading Cycloclasticus (Berthe-Corti and Nachtkamp 2010).

Despite the bacterial genera comprised in the OHCB group, other genera have been reported as hydrocarbon degraders in seawater.

Microbacterium and Porphyrobacter strains were isolated from enrichments containing benzo[a]pyrene. Also, strains belonging to the genera Vibrio, Marinobacter, Cycloclasticus, Pseudoalteromonas, Marinomonas, and Halomonas were reported isolated from sediments and able to grow on phenanthrene or chrysene (McGenity et al. 2012). Recently, PAH degraders were isolated from a Brazilian marine oil terminal (TEBAR), including Idiomarina sp. R2A 23.10, able to degrade phenanthrene; Marinobacter flavimaris R2A 36.J, able to degrade pyrene; and Modicisalibacter tunisiensis MOD 31.J, able to degrade phenol (Gomes et al. 2018). Dietzia maris, Micrococcus sp., and Bacillus sp. were also related with hydrocarbon degradation in marine environments (Dellagnezze et al. 2014; Kleinsteuber et al. 2006; Nakano et al. 2011). In addition, members belonging to some fungal genera, including Aspergillus, Mucor, Fusarium, and Penicillium, have been reported as capable to degrade petroleum (Xue et al. 2015).

5.3.4 Contamination in Terrestrial Environments

Oil spill affecting soil is one of the major global concerns today. Petroleum contamination of soil causes serious hazards to human health and pollution of groundwater and surface water bodies, which limits their use and decreases agricultural productivity, resulting in obvious economic losses. Health risks that emerge from direct contact with the contaminated soil and secondary contamination of water supplies are the major concerns (Thapa et al. 2012). Terrestrial spills tend to be from pipelines, railway accidents, and tank storage. The spread and pathway of oil spilled in terrestrial environments depends on the type of terrain, soil, and vegetation. Moreover, oil (or its derivatives as volatile monoaromatic compounds) can seep through soil and migrate to groundwater or even attach to soil particles. Subsurface contamination is thus affected by soil/sediment characteristics as grain size and by oil features as viscosity and weathering state (Pearson and Fleece 2014).

In addition, volatile organic compounds (VOCs), mainly BTEX compounds (benzene, toluene, ethylbenzene, and xylene), have been considered as major contributors to the deterioration of water and air quality. BTEX are prevalent in the environment as consequence of combustion processes as well as vehicle exhausts. They are also used as industrial solvents for the synthesis of several organic compounds (e.g., plastics, synthetic fibers, and pesticides) and are present in many petroleum derivatives (El-Naas et al. 2014).

Another ecosystem constantly threatened by petroleum contamination is intertidal wetlands. Environments such as salt marshes and tropical mangroves play a crucial role in life cycle of many species. Besides high primary productivity, these environments function as protection barrier from wave and storm damage, provide food and shelter for fish and other marine species, and help dissipate greenhouse gases. Nevertheless, these environments are extremely susceptible to oil input, not only by receiving oil-contaminated seawater but also due to their proximity to oil refineries and industries (McGenity et al. 2014).

Mangrove sediments can retain pollutants increasing their toxicity and impacting the ecosystem integrity. Petroleum compounds are the most damaging, and in addition to the type, concentration, and weathering of oil, climatic and tide conditions may worsen the mortality of the ecosystem. In case of severely harmful oil spill, causing even the death of vegetal species and trees, oil degradation in sediments can be diminished and remediation alternatives are needed (Santos et al. 2010).

Recent mangrove studies have focused on microbial indicators of hydrocarbon pollution on mangrove ecosystems. The interaction dynamics among key groups represents an important parameter to evaluate pollution and its mitigation. Santos and collaborators (2011) carried out a study at Marambaia mangrove (Rio de Janeiro, Brazil) based on 454 pyrosequencing of 16S rRNA amplicons to identify candidate indicator groups in contaminated and pristine sediment samples. The authors showed that some groups as Cycloclasticus, Marinobacter, and Marinobacterium can thrive in the oil presence, whereas others like the members belonging to the order Chromatiales and the genus Haliea are much more sensitive to it. This work enlarged the understanding about microbial indicators of oil pollution in mangroves. In another study, the presence of specific bacterial groups was correlated with the distribution of petroleum pollutants, corroborating that bioindicators of oil pollution can be used as a suitable tool to better analyze contamination (Ghizelini et al. 2012).

5.3.5 Petroleum Contamination in Cold Environments

Areas contaminated with petroleum hydrocarbon in polar environments as Antarctic and Arctic represent a serious environmental problem. The management of contaminated sites in these regions faces challenges naturally associated with intrinsic environmental conditions. Several technologies have been improved and adapted for in situ application in these regions, as bioremediation (bioaugmentation and biostimulation), landfarming, biopiles, and others. However, the choice of the most suitable treatment strategy takes into consideration several aspects, as climate and soil characteristics, costs, environmental regulations, logistics, and infrastructure (Camenzuli and Freidman 2015).

Oil degradation and bioremediation efficiency under cold conditions are mainly dependent on temperature, which influence several parameters as chemical composition of oil; rate of hydrocarbon degradation; bioavailability of compounds, nutrients, oxygen rate (aerobic conditions), or other electron acceptors (anaerobic conditions); and also composition and abundance of microbial communities (Yang et al. 2009).

Parameters that influence the biodegradation process in Arctic soils are similar to those in marine and terrestrial environments, such as climate conditions, features of the soil and oil, costs, infrastructure, and environmental regulations (Naseri et al. 2014, Yang et al. 2009).

Based on the quoted authors, such parameters are described in detail below:
  • Type of hydrocarbons: Molecular structure of compounds influences their biodegradation rates.

  • Bioavailability: Temperature, oil viscosity, water solubility, amount of spilt oil, and soil characteristics influence hydrocarbon bioavailability. For example, during winter, when the soil pore water is frozen avoiding the transfer of nutrients, oxygen, and hydrocarbon molecules, bioavailability is critical.

  • Cold-adapted, oil-degrading microorganisms: To achieve an effective biodegradation process, microbial degraders must be suitable and resist environmental changes.

  • Soil temperature, nutrient levels, and humidity: Low temperature affects oil weathering processes and influences the metabolic activity of hydrocarbon degraders, inhibiting biodegradation process or reducing it at extremely low rates for most of the year in polar soils. Also, in cold conditions, rate of nutrient recycling decreases in the ecosystem, resulting in a scarcity of nitrogen and phosphorous. In the same way, soil humidity can influence the biodegradation rate due to its effects on hydrocarbon bioavailability and also the transfer and diffusion process of other materials, such as gases and nutrients.

Biostimulation and bioaugmentation have been studied and applied in cold environments (Kasanke and Leigh 2017; Wang et al. 2015; Margesin and Schinner 2001), as well as other bioremediation approaches, like biopiles and landfarming (Camenzuli and Freidman 2015). Moreover, soil warming or heat injection can be carried out through engineered biopiles, in order to achieve optimal temperature. However, excessive heat leads to the evaporation of soil pore water, which decreases hydrocarbon bioavailability. To circumvent this limitation, the use of humidified air is recommended, as well as water that must be provided during the process to equalize the dry portions (Naseri et al. 2014).

5.4 Bioremediation Studies and Practical Aspects

As previously described, bioremediation involves different approaches aiming at the mineralization of organic compounds by using microorganisms or their products.

A recent example of natural attenuation (in situ bioremediation) was observed after the Deepwater Horizon (British Petroleum) platform explosion accident, quoted previously. Hazen et al. (2010) evaluated deep water samples from across the Gulf of Mexico aiming the comprehension of the impact of the deep hydrocarbon plume on the marine microbes and the rates of hydrocarbon biodegradation. They reported a shift in the marine bacterial community exposed to the oil, with an increase in the abundance of microorganisms from the order Oceanospirillales (class ϒ-Proteobacteria), suggesting a faster acclimation and ability of such bacteria to thrive in the oil.

To be an effective process, biostimulation is dependent on availability and capability of intrinsic microorganisms to perform the complete degradation of a target pollutant. Still, the amount of specific degrading groups (in colony forming units – CFU/mL or gram of soil) must be abundant (Luqueño et al. 2011). Liu and co-workers (2010) reported the use of biostimulation in polycyclic aromatic hydrocarbons (PAH) contaminated soil by the addition of organic fertilizer. After 360 days, there was a reduction of 58% PAH in the amended treatment when compared to the control without any fertilizer. Moreover, the authors observed a smaller number of degrading bacteria in the control samples than in the treated ones and concluded that at concentrations below 105 UFC g−1, bioremediation process may not occur significantly. Thus, the higher the abundance of degrading microorganisms within an area under remediation treatment, the faster and more efficient the process is.

Other works have reported the use of biostimulation approach whether in both soil and aquatic environments, resulting in an effective removal of pesticides (Kanissery and Sims 2011), PAH and petroleum (Nikolopoulou and Kalogerakis 2008; Nikolopoulou and Kalogerakis, 2009; Delille et al. 2009; Yu et al. 2011), and organohalogenates (Major et al. 2002).

In some cases, bioaugmentation is considered as an alternative remediation technique when biostimulation or natural attenuation fails. This may happen when (1) there is low abundance of degrading microorganisms in the treated area and (2) the native microbiota do not present physiological capability to degrade pollutants (Fantroussi and Agathos 2005; Tyagi et al. 2011).

There are different strategies of bioaugmentation, as follows: (1) reinoculation of potential oil degraders from autochthonous microbial community, (2) selection of suitable target microorganisms from contaminated environments similar to the target area to be treated, and (3) use of genetically modified microorganisms (GMO) aiming to potentiate the degradation process (Mrozik and Piotrowska-Seget 2010, Hosokawa et al. 2009). Hosokawa et al. (2009) reported the bioaugmentation approach using ABA (autochthonous bioaugmentation) in Hokkaido Island in petroleum-contaminated sediments, comparing different consortia. The consortium previously isolated from contaminated sediment showed higher efficiency to degrade petroleum compounds.

Several bacterial and fungal strains have been used by different authors in bioaugmentation strategies for petroleum and derivative compounds (Table 5.4).
Table 5.4

Microorganisms used in bioaugmentation approach for degradation of diverse pollutants from petroleum and derivatives

Microorganism

Compound

References

Alcanivorax

Petroleum hydrocarbons

McKew et al. (2007), and Gertler et al. (2009)

Bacillus

Diesel oil; quinolone

Bento et al. (2005) and Tuo et al. (2012)

Rhodococcus

Diesel oil; PHA

Kuyukina and Ivshina (2010) and Lee et al. (2011)

Pseudomonas

Petroleum; simazine

Stallwood et al. (2005), Morgante et al. (2010), and Mei-Zhen et al. (2012)

Burkholderia

Carbofuran; ethylenediaminetetraacetic acid (EDTA)

Chen et al. (2005) and Plangklang and Reungsang (2011)

Aspergillus

Anthracene, naphthalene (PAH)

Ye et al. (2011) and Ali et al. (2012)

Penicillium

Petroleum/crude oil

Ojeda- Morales et al. (2013), and Crisafi et al. (2016)

Despite several advantages in bioaugmentation, as low cost and high efficiency, there are some limitations involved in its application. Strain selection, microbial ecology aspects, and inoculation procedure may influence directly in the process effectivity. Parameters such as availability and amount of water, oxygen, nitrogen, and phosphorus and, on top of that, the ability of microorganisms to degrade the target contaminants and compete/act synergically with autochthonous microbiota are essential factors to achieve a complete degradation of the pollutant. Remediation process under natural conditions may be inefficient in absence of any of the abovementioned parameters (Boopathy 2000; Tyagi et al. 2011). Gentry (2004) reported some methods that may enhance the activity of exogenous microorganisms or genes in the environment: (1) development of methods to enhance the tolerance and resistance of exogenous microorganisms into contaminated areas, (2) research for genetically engineered microorganisms with remediation potential, (3) monitoring of the activity and/or presence of introduced microorganisms through reporter genes, and (4) control of the released genetically engineered microorganisms through suicide genes.

The combined use of biostimulation and bioaugmentation for hydrocarbon removal is mentioned in previous literature and may be a useful approach for accelerating bioremediation. Exogenous and indigenous microorganisms can be supported from biostimulation due to nutrient addition and electron acceptors (El Fantroussie and Agathos 2005).

Yu and collaborators (2005) reported the degradation of a mixture of three types of polyaromatic hydrocarbons (PAH) in mangrove sediments, fluorene (Fl), phenanthrene (Phe), and pyrene (Pyr), using three approaches individually: natural attenuation, biostimulation, and bioaugmentation during 4 weeks. At the end of the last week (week 4), natural attenuation (only autochthonous microorganisms) removed more than 99% of fluorene and phenanthrene but only about 30% pyrene. Biostimulation, adding mineral salt medium allowed more than 97% degradation of all three PAHs, showing that nutrient amendment could enhance pyrene degradation. However, bioaugmentation, using a PAH-degrading bacterial consortium enriched from mangrove sediments, was not able to stimulate PAHs degradation, and biodegradation percentages were similar to those obtained by natural attenuation.

Crisafi et al. (2016) reported the treatment of oil-contaminated seawater after an oil spill event occurred in the Gulf of Taranto (Italy), using different bioremediation approaches. The authors concluded that biostimulation based on inorganic nutrients allowed 73% hydrocarbon biodegradation; bioaugmentation using selected hydrocarbonoclastic consortium composed by Alcanivorax borkumensis, Alcanivorax dieselolei, Marinobacter hydrocarbonoclasticus, Cycloclasticus sp. 78-ME, and Thalassolituus oleivorans allowed approximately 79% degradation, while the addition of nutrients and a washing agent allowed 69% degradation. Nevertheless, the authors also could observe harmful effects of the washing agent on the microbial community.

5.5 Bioaugmentation Using Genetically Engineered Microorganisms (GEM)

Almost 40 years ago (in the decade of 1980), the search for bacterial genes encoding catabolic enzymes for degradation of recalcitrant compounds gained attention, along with their cloning and genetic characterization, increasing global interest toward the metabolic potential of microorganisms for biodegradation processes. The first genetic study on microbial degradation was performed with a Pseudomonas strain developed to degrade several compounds such as camphor, octane, salicylate, and naphthalene (Chakrabarty 1972; Chakrabarty et al. 1973). This work resulted in a patent [US Patent #425944] (Cases e De Lorenzo 2005).

GEM might be a useful biological tool to treat polluted environment. Biodegradation rates of several contaminants could be enhanced by genetic engineering through cloning of genes involved in degradation pathway(s) with wider substrate specificities. However, the critical point before the release into the environment is to check the stability of any GEM. In addition, the competence to thrive in natural environments can determine the fate of released GEM (Samanta et al. 2002).

Nevertheless, the use of GEM for bioremediation faces restrictive legislation that forbids in situ application. However, using GEM for bioremediation purposes might be a viable and effective alternative, including the performance and degradation time, and it could be considered in containment conditions (de Lorenzo 2010).

5.6 Marketable Bioremediation Agents

The United States Environmental Protection Agency (US EPA) considered as bioremediation agents microbiological cultures, enzymes, or nutrient additives, which can boost biodegradation processes and mitigate contaminated areas. In the year 2001, the same agency compiled a list of 15 bioremediation agents in the scope of National Oil and Hazardous Substances Pollution Contingency Plan (NCP) Product Schedule, and in the next year, this list was modified, totalizing only 9 bioremediation agents. Several new companies have strengthened commercial products in order to clean and treat contaminated environments whether using lyophilized microbial consortia or their enzymes or metabolites, like biosurfactants or other polymers, which currently tend to be a growing market (Randhawa and Rahman 2014).

However, studies have reported that the efficiency of bioremediation products may vary between laboratory and field conditions. Due to the limitation to simulate environmental conditions in laboratory tests (biological interactions, influence of abiotic effects, such as climate and nutrient mass transport), the biological product may fail in the field application. For this reason, field studies are required as the final step to testify the effectiveness of bioremediation products (Das and Chandran 2011).

A recent review provides a list of bioremediation companies all over the world, such as the German “AB enzymes” and the American “EOS Remediation” among others, which are also involved in development of biosensors for detecting pollutants (Mahmutoglu et al. 2010).

Along with emerging bioremediation companies, researchers have developed several methods in order to restore contaminated sites. Based on Thomson Innovation patent database, the work carried out by Kapoor and co-workers (2013) analyzed a total of 125 patent applications and their approaches involving oil-degrading microorganisms to achieve bioremediation. Still, in a rank for bioremediation technology, the United States of America is the leading country followed by China, Korea, Japan, and Russia. Several companies worldwide known for developing innovative approaches currently work toward eco-friendly products and sustainable solutions, including DuPont, Biosaint, and others.

5.7 Conclusion

In conclusion, given the increasing number of patents and companies all over the world, bioremediation is not a mere theoretical scientific concept but a concrete and applied efficient tool to treat polluted environments, ensuring a minimum impact on the ecosystem. Moreover, this scenario opens the possibility to uncover new technologies and approaches that may be used individually or in combination, as well as the improvement of known practices, aiming at eco-friendly treatments for environment decontamination and waste management in general.

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Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Bruna Martins Dellagnezze
    • 1
  • Milene Barbosa Gomes
    • 1
  • Valéria Maia de Oliveira
    • 1
  1. 1.Division of Microbial Resources, Research Center for Chemistry, Biology and Agriculture (CPQBA)Campinas UniversityCampinasBrazil

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