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diation &

me B
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Paniagua-Michel and Rosales, J Bioremed Biodeg 2015, 6:2
Journal of
urnal of Bio

iod
DOI: 10.4172/2155-6199.1000273
egradation
Bioremediation & Biodegradation
Jo

ISSN: 2155-6199
ISSN: 2155-6199

Research
Review Article
Article Open
OpenAccess
Access

Marine Bioremediation - A Sustainable Biotechnology of Petroleum


Hydrocarbons Biodegradation in Coastal and Marine Environments
Paniagua-Michel J* and Alberto Rosales
Department of Marine Biotechnology, Center for Scientific Research and Higher Education from Ensenada BC Mexico (CICESE), Km 107 Carretera Tijuana-Ensenada,
Ensenada, BC, Mexico

Abstract
Bioremediation is now the best successful initiative to mitigate and to recover sites contaminated with
hydrocarbons and has been the preferred process for clean-up contamination around the oceans of the world. The
advantages of marine microorganisms in the removal of petroleum hydrocarbons, exemplifies the eco-sustainable
bioremediation that can be achieved in sensitive marine environments and probably until now the only approach for
biodiversity rich and fragile environments. The use of bio-surfactants to protect the marine environment is particularly
attractive since a number of marine bacteria and microalgae strains can produce bio-surfactants during growth
on hydrocarbons. Moreover, according to recent results, marine microorganisms, exhibit the maximum yield and
surface-active property compared to terrestrial species. Because of the interest to find ecofriendly solutions for
the bioremediation and biodegradation of petroleum hydrocarbons in the marine environment, the use of marine
microorganisms and their respective bio-surfactants is preferable to that non-marine and of synthetic origin. The aim
of this review is to integrate the advantages of marine bioremediation coupled to hydrocarbon removal from marine
environments. This alternative of bioremediation is a natural process of waste treatment, relatively cost-effective
than other remediation approaches that are used for clean-up of hazardous waste in coasts, seas and oceans that
can be adaptable to variable environmental conditions, viz, estuarine, coastal and marine pollution and is widely
accepted by the society.

Keywords: Bioremediation; Biodegradation; Petroleum, bioremediation a sustainable and environmentally eco-friendly


Hydrocarbons; Marine; Bio-surfactant approach for cleanup-polluted environments [8]. Moreover, given
the difficulties of the level and the scale in marine areas, very little
Introduction practical bioremediation and restoration has been carried out for
Petroleum-derived products are the major source of energy open marine systems [6,9]. The physical, chemical and mechanical
for industry and societies. The transport of petroleum across the technologies to remove petroleum hydrocarbons from contaminated
world represents a frequent and potential for oil spills in the marine marine environments in most of the cases are unsustainable and
environment [1]. Actually, it is widely recognized that petroleum can be expensive. Bioremediation is a cost-effective and sustainable
hydrocarbons contamination has impacted, and damaged the world biotechnology for the treatment of contaminated coastal and marine
oceans, seas and coastal zones and represent a constant threat to the sites. This biotechnology utilize living cells or biological components
planet Earth health sustainability [2]. to complete biodegradation of complex organic contaminants to other
simpler organic compounds into carbon dioxide, water, inorganic
The recent catastrophe and sequels remnants after approximately
compounds, and cell protein [10,11]. The objective of this review is
600,000 tons of crude oil hydrocarbons released by the Deep-water
to update the current status and potentials of marine bioremediation
Horizon explosion in the Gulf of Mexico, has increased the volume
as a sustainable alternative for impacted fragile and sensitive marine
of petroleum enters the marine environment each year (~ 1.3 million
environments.
tons). That scenario and the past oil spill accidents in oceans at large
scale and the continuous anthropogenic negligence in coastal seas and Advantages of marine bioremediation and biodegradation of
Bays, has also contributed to renovate the world public awareness on petroleum hydrocarbons
the magnitude of the environmental damage [3,4].
In marine environment, bioremediation is considered as the most
At small scale, productive environments and biota are highly effective and attractive cleaning biodegradation biotechnology to
impacted, especially in low-energy habitats, such as lagoons and salt
marshes. Marine biotechnology is a technology of the Century to
*Corresponding author: Paniagua-Michel J, Department of Marine Biotechnology,
contribute to the sustainable development of our planet. The growing Center for Scientific Research and Higher Education from Ensenada BC Mexico
pressure on our natural resources by the increasing population growth (CICESE), Km 107 Carretera Tijuana-Ensenada, Mexico, Tel: +52-646-1745050;
and pollution also has impacted the planet on water and land resources. E-mail: [email protected]
Contaminated coastal and marine environment, generally result from Received January 03, 2015; Accepted January 28, 2015; Published January 30,
the continuous carelessness and negligence of anthropogenic activities 2015
on the former unlimited abundance of land and marine resources Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A
of early times [5]. The increasing need to remedy adverse effects of Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-
anthropogenic activities on estuarine, coastal and marine ecosystems 6199.1000273
[6], has prompted the development of effective bioremediation strategies
Copyright: © 2015 Paniagua-Michel J, et al. This is an open-a ccess article
[7]. Nevertheless, probably one of the main interests of bioremediation distributed under the terms of the Creative Commons Attribution License, which
is its compatibility with the major natural biogeochemical cycles and permits unrestricted use, distribution, and reproduction in any medium, provided
the original author and source are credited.
recycling routes of the earth and marine ecosystems, which make

J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273
Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-6199.1000273

Page 2 of 6

decrease the level of pollution and to recover contaminated marine dilute, dispersed or widely diffused contaminants of seawater and can
environments [11]. The technology of bioremediation relies on the use often be carried out on site, in situ, and ex-situ.
of the diverse metabolic capabilities of microorganisms or their parts
In addition, probably most important is it noninvasive nature
for the degradation and removal of many environmental pollutants without causing a major disruption of normal activities. The
[10,12]. Bioremediation is widely applied due to the increased practical Bioremediation approaches can prove less expensive, and relatively
approaches of natural attenuation and biodegradation, in most natural cost-effective than other remediation approaches that are used for
marine sites [11]. The following bioremediation approaches are usually clean-up of hazardous waste in coasts, seas and oceans [7,13].
applied in marine environments impacted by an oil spill, (i) addition
of oil degrading bacteria to supplement or to enrich the existing Biodegradation of petroleum hydrocarbon contaminants in
microbial biota, which is called bio-augmentation; and (ii) application coastal-marine environments
of fertilizers (nutrients), to encourage and stimulate the growth of
Bioremediation is an efficient degradation technology that is
indigenous oil degraders, that is named bio-stimulation [10]. currently used to remove hydrocarbons from contaminated sites,
The actual most contaminant and emerging problems in polluted since mechanical, physical and chemical treatments have limited
saline and marine waters can find solution by bioremediation, e.g. effectiveness [10]. Bioremediation exerts its action on biodegradation.
aquaculture and fisheries effluents, trace metals, endocrine disrupters, Biodegradation by natural populations of microorganisms represents
mixed waste/ municipal wastewaters discharges, crude and refined oil one of the primary and natural mechanisms by which petroleum and
pollution, as well as biological carbon sequestration. Bioremediation has other hydrocarbon pollutants can be processed, bio-transformed and
now been the best successful initiative to remediate sites contaminated in removed from the environment. However, the passiveness and slow
the sea with hydrocarbons or other specific contaminants and has been action of natural biodegradation in order to be effective require be
complemented by other bioremediation measures. In this context,
the preferred process for clean-up contamination around the oceans of
the ability to establish and maintain conditions that favor enhanced
the world. However, under certain critical situations, interfering factors,
oil biodegradation rates in the contaminated environments is a major
can reduce the efficient achievement and removal of pollutants. Among
factor to be considered.
these factors, we can list the following: the nature of the contaminant
(s), structure, water solubility, bioavailability, biodegradability, co- Any biodegradation action in the marine environment must to
metabolism potential, substrate/metabolite concentration, and toxicity, understand how hydrocarbons are degraded by microorganisms, and
the properties of the seawater, nutrients, oxygen, salinity, presence of thereby mitigate ecosystem damage. It is known that crude oils and
bioavailability enhancing agents, temperature, pH and, and the activity refined products are mostly composed of biodegradable molecules,
of the microbial population [13]. The alternative of bioremediation is a whose decomposition from the environment depends as they are
natural process of waste treatment widely accepted by the society that consumed by microbes [14]. Once the hydrocarbons are released
can be adaptable to variable environmental conditions, viz, estuarine, in seawater, several processes occur, which can contribute to the
coastal and marine pollution. The residues of the treatment are usually bioremediation and biodegradation in the marine ecosystem (Figure
harmless products and include carbon dioxide, water, and cell biomass 1).
[7]; the remained residues of the biodegradation can be recycled, and In the case of shorelines, saltmarshes and beaches, successful
regenerated into more cell biomass in the respective environments to be bioremediation field trials have been reported. At higher oil
implemented (coastal, estuarine, and extreme marine environments). concentrations, oxygen plays an important role for the achievement
The bioremediation treatment can be performed in conditions with of successful bioremediation. When oil had penetrated into the anoxic

Figure 1: Main mechanisms involved in the aerobic biodegradation of petroleum hydrocarbons in the marine environment (modified after [10]).

J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273
Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-6199.1000273

Page 3 of 6

layer of sediments, oxygen additions is a common bioremediation an important role in hydrocarbon degradation and bioremediation.
strategy, in order to overcome oxygen levels depletion. In addition, in The quality and quantity of available nitrogen and phosphorus in
programs of salt marshes recovery, it may be feasible to bio-remediate seawater affects the growth and activities of hydrocarbon-degrading
oil-contaminated fine sediments by using nutrient and oxygen microorganisms mostly in a marine environment. These nutrients
amendments [15]. Among the complementary programs, additions acts as fertilizers to an oil-contaminated marine environment and can
of lyophilic sources of nutrient may encourage biodegradation on the stimulate the biodegradation of spilled oil, as was the action undertaken
surfaces of rocks under proper bioremediation schemes. The strategic in the large-scale application for bioremediation after the oil spill
plan to bio-remediate oil spilled on the shorelines is to treat first the oil from the Exxon Valdez in Alaska [1]. Despite many microorganisms
that is sorbed to beach sediment. It is suggested that bioremediation capable of degrading petroleum components have been isolated, only
approaches works better after physical removal of oil; hence, few of them have been tested and reported as successful when applied
biodegradation should be focused on the oil remaining on the beach for petroleum biodegradation in marine environments. The case of
after other processes are largely complete. This approach could be Alcanivorax spp., frequently associated in oil-contaminated marine
widely applied to different shoreline types. The presence of hydrocarbon habitats has been reported as successful in biodegradation studies.
degrading microorganisms play an effective role in Bioremediation
of any spilled hydrocarbons in the contaminated environment.
Hydrocarbon degraders are ubiquitous in the marine environment.
The presence of a single microbial species, which can degrade only one
or two classes of hydrocarbon within a crude oil, reduce significantly
the kinetics of bioremediation [15]. In such circumstances, consortia of
microorganisms are required to significantly biodegrade a large fraction
of crude oil. In cases where the indigenous microflora is deficient in
hydrocarbon-degrading potential, the strategy of bioaumentation can
be a good option. Hence, seeding of active degraders will depend of
the respective environmental condition. The use of allochthonous
microorganisms and its degradative efficiency in the contaminated
ecosystem will depend of several factors. For example, the prevailing
environmental parameters on the selected site for bioremediation play
an important role, viz, oxygen, salinity, pH, temperature, nutrient
quantity and quality. For instance, environmental conditions related
to the site to be remediated plays a key role in the successful program
of bioremediation. For instance, pH of the site is an important factor to
consider according to the requirements of the added microorganisms
(particularly for salt marshes) or adaptations of the organisms to the
tidal cycles, the salinity, or the oligotrophic conditions of many beach
environments [15].
Keeping aerobic conditions ensure rapid and complete degradation
of petroleum hydrocarbons [16] as shown in Figure 2. The initial Figure 2: Biodegradation processes of oil in the marine environment.
oxidative process is carried out by oxygen, which activate enzymatic
key intracellular reaction by the catalytic action of oxygenates. The
different degradation pathways lead to intermediates of the central
intermediary metabolism, viz the tricarboxylic acid cycle. Lately, cell
growth and biosynthesis of biomass occurs from the central precursor
metabolites [10]. Apart of this mechanism, the production of bio- plays
also a key role in hydrocarbon biodegradation [17,18] as explained
down lines and shown in Figure 3. During the last couple of decades,
bioremediation has been part of the programs of effectively restore and
recovery of polluted marine sites. The complex composition of crude
oil, mostly constituted from thousands of components, viz, saturates,
aromatics, resins and asphaltenes [1] difficult its treatment. Upon
discharge into the sea, hydrocarbons are exposed to weathering, which
produces the combined effects of physical, chemical and biological
modification. That is why; the first molecules degraded in the marine
environments are especially those of smaller molecular weight such as
saturates hydrocarbons, which are readily biodegraded. The presences
of aromatics compounds with one, two or three aromatic rings, which
are abundant in marine environments, are also efficiently biodegraded.
Nevertheless, compound’s with higher number of aromatic ring (>4) are
recalcitrant and quite resistant to biodegradation. In such situation are
Figure 3: Mechanisms of hydrocarbon removal by biosurfactants depending
asphaltenes and resin fractions, which contain higher molecular weight on their molecular mass and concentration [37].
compounds [1]. Nutrients, especially nitrogen and phosphorous plays

J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273
Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-6199.1000273

Page 4 of 6

The fertilization in situ by enrichments of nitrogen and phosphorus, particularly attractive since a number of marine bacterial and microalgae
undertaken to stimulate the growth of bacteria, also produces at the strains can produce bio-surfactants during growth on hydrocarbons
same time, an increase in the endogenous biodegradation capabilities [17,18]. Moreover, according to Maneerat [24] microorganisms of
of petroleum hydrocarbons [1]. marine origin, exhibit the maximum yield and surface-active property
compared to terrestrial species.
Biodegradation of petroleum hydrocarbons in marine environments
are influenced by salinity and temperature. These parameters affect Because of the interest to find ecofriendly solutions for the marine
the structure and physiology of existing microbial communities and environment, the use of bio-surfactants is preferable to those of
modify the solubility and viscosity of the pollutants. As long as the synthetic origin. However, scarce information on either bio-surfactant
environmental conditions become extreme, a decrease in the metabolic produced by marine microorganisms or bio-surfactants active in saline
potential and diversity of degrading bacteria is observed [19,20]. water has been reported so far. In order to effectively work in removal
Concerning the structure of the pollutants, a remarkable inhibitory of petroleum hydrocarbons, the following environmental conditions
effect of salinity was observed for aromatic than for aliphatic compounds are aspects to be considered: salinity, pH, temperature and pressure
[21]. At salinities higher than 20%, Marinobacter hydrocarbonoclasticus [30,31]. Among microorganisms, only bacteria and microbial consortia
degraded various aliphatic and aromatic hydrocarbons [22]. Halophilic have been probed as effective in the practical removal of hydrocarbons
Marinobacter-dominant culture isolated from an oil production facility from seawater, but the cases of yeasts, algae and protozoa still are under
in Oklahoma, shown degradation capacities for benzene, toluene, ethyl research with highly promising potentialities [17,18,30].
benzene, and xylenes (BTEX) completely at 14% salinity [23]. The
Biodegradation of hydrocarbons by native microbial populations
biodegradation of petroleum compounds at different salinities by mat
is the primary mechanism by which hydrocarbon contaminants are
microorganisms of the Arabian Gulf coast of Saudi Arabia showed
removed from the environment. Hence, biosurfactants are capable
the bioremediation potential of these mats developed on polluted oil
of increasing the bioavailability of poorly soluble polycyclic aromatic
environments. In these conditions, pristine and n-octadecane were
hydrocarbons such as phenanthrene [32].
optimally degraded at salinities between 5 and 12% (weight per volume
NaCl). The optimum degradation of phenanthrene was at 3.5% salinity, However, the addition of biosurfactants has been reported
and 8% for dibenzothiophene and 28-401°C for both aliphatics and as stimulant of the indigenous bacterial population to degrade
aromatics [19]. hydrocarbons at rates higher than those which could be achieved
through addition of nutrients alone [25]. A successful bioremediation
Marine bio-surfactants: an effective role in bioremediation at large scale was reported on the Exxon Valdez oil spill. In such case, the
and biodegradation of Petroleum Hydrocarbons in Marine application of Rhamnolipid from P. aeruginosa, exhibited significant
environments removal capacities for oil from contaminated Alaskan gravel [33,34].
The structurally diverse group of surface-active metabolites, In another experiment, 56% of the aliphatic and 73% of the aromatic
synthesized by microorganisms, is classified as bio-surfactants [24,25]. hydrocarbons were recovered from hydrocarbon-contaminated sandy-
The bio-surfactants produced by some marine microorganisms are loam soil by treatment with P. aeruginosa biosurfactant [25].
promising agents for bioremediation of hydrocarbons, particularly Most of the biosurfactants are anionic or nonionic; the structure is
of oil pollution in marine environments [24]. Because of the reduce a characteristic of the microorganism producing the surfactant under
surface and interfacial tensions exerted by these molecules, in both the specific growth conditions [26,35,36].
aqueous solutions and hydrocarbon mixtures, makes them potential
candidates for enhancing oil recovery [25], and actually are under In oil- polluted saline environments, biosurfactants from halophilic/
intense research, particularly for the bioremediation of the sea polluted halotolerant microorganisms play a significant role in the accelerated
by crude oil. The property of microorganisms to accumulate bio- remediation of these environments. Probably the major advantage of
surfactants on the cell surface and adheres to hydrocarbon self-define biosurfactants is their property to induce relaxation or attenuation of
the microbial cell itself as a bio-surfactant. surface tension, which increase solubility and enhances degradation of
hydrocarbons as exemplified in Figure 3 modified from Pacwa, et al.
Most of the microbial surfactants are lipid in nature and grouped [37], which exhibit the different mechanisms of hydrocarbon removal
into glycolipids, phospholipids, lip peptides, natural lipids, fatty acids by biosurfactants depending on their molecular mass and concentration
and lipopolysaccharides [26,27]. Bio-surfactants are amphipathic in aqueous media. Microbial production of a surfactant derived from
molecules with a hydrophilic and a hydrophobic domain, which trehalose by marine species as the case of Rhodococci proved successful
facilitate the uptake of hydrocarbons into cells [28]. Bio-surfactants for n-alkanes removal [38]. These kinds of applications could have
offer attractive properties and products in petroleum-related activities important roles as surface-active agents for in situ bioremediation of
and industries for use in enhanced oil recovery, in cleaning oil spills, fragile and sensitive environments anchoring a high biodiversity as in
in oil emulsification, and in breaking industrially derived oil-in-oil the case of marine environments. For instance, strains able to degrade
emulsions. n-alkanes (C10–C30) in the presence of 30% (w/v) NaCl actually are
Bio-surfactants exhibit three major characteristics of surface-active a reality [18]. Moreover, brines removal from industrial activities
agents, such as: (i) enrichment at interfaces, (ii) lowering interfacial (agricultural, wastewater treatment-desalinization, salt production,
tension and (iii) micelle formation. The industrial advantages of these etc.) can be successfully treated with the use of exopolysaccharides
over the chemical surfactants were reported as following: lower toxicity (EPS) produced and supported by marine organisms as well as with the
[29], higher biodegradability; better environmental compatibility; use of heterotrophic and halophilic bacteria for the treatment of hyper
high selectivity and specific activity at extreme temperatures, pH and saline wastewaters. A main and surrogated role of EPS in Cyanobacteria
salinity resistant [25]. and certain microbial consortia and organisms from coastal –
marine environments have been reported as able to metabolizing oil
The use of bio-surfactants to protect the marine environment is hydrocarbons, a condition that is enhanced by pollutant substrate

J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273
Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-6199.1000273

Page 5 of 6

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J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273
Citation: Paniagua-Michel J, Rosales A (2015) Marine Bioremediation - A Sustainable Biotechnology of Petroleum Hydrocarbons Biodegradation in
Coastal and Marine Environments. J Bioremed Biodeg 6: 273. doi:10.4172/2155-6199.1000273

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J Bioremed Biodeg
ISSN: 2155-6199 JBRBD, an open access journal Volume 6 • Issue 2 • 1000273

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