**2. Type of pollutants**

#### **2.1 Polycyclic aromatic hydrocarbons (PAHs)**

Polycyclic aromatic hydrocarbons (PAHs) are a group of common environmental contaminants that are especially widely detected in the aquatic environment categorized as general environmentally harmful pollutants [15]. PAHs typically enter the environment through the natural sources and anthropogenic sources. Examples of

*Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

**Figure 2.** *Sources of PAHs, types of PAHs and their effects on humans.*

natural sources of PAHs formation include volcanic eruptions, forest fires, decaying organic matter, natural petroleum, plant synthesis, rare minerals, anthropogenic sources of PAHs such as domestic sources (burning coal, oil, gas, wood, garbage and cigarette), industrial sources (sewage sludge and organic waste), and agriculture sources (pesticides, formulation, and burning residuals) [3, 16, 17].

PAH compounds contain only carbon and hydrogen atoms. Chemically the PAHs are comprised of two or more benzene rings bonded in linear, cluster or angular arrangements [17]. PAHs form up to six fused aromatic rings are often referred to as small PAHs, and those containing more than six aromatic rings are called large PAHs [3, 17]. Such molecular arrangements are illustrated in **Figure 2**.

PAHs are hydrophobic compounds that degrade hardly in water and sediment. Due to their hydrophobicity, they are transferred into cells and induce gene expression of the cytochrome P450 (CYP) enzyme group [18, 19]. They have been shown to have carcinogenic and mutagenic effects and are strong immune suppressants. In addition, toxicological studies have revealed other types of PAH toxicities such as developmental toxicity, genotoxicity, immunotoxicity, oxidative stress and endocrine disruption. Because of their ubiquity in the natural environment and various harmful effects on organisms, PAHs are among the most concerning organic pollutants, and The Environmental Protection Agency has introduced these compounds as hazardous contaminants [20, 21].

#### **2.2 Heavy metals**

Heavy metals (HMs) are considered one of the most important inorganic pollutants in marine environments which the extensive use and distribution of them has increased rapidly all over the world [22]. They are usually released through human activities such as industrial operations, agriculture activities, mining, electroplating, electronic waste/E-waste and geological sources include volcanic eruptions, weathering of metal-containing rocks, sea-salt sprays, forest fires and natural weathering processes [22, 23].

Among heavy metals magnesium (Mg), nickel (Ni), chromium (Cr3+), copper (Cu), calcium (Ca), manganese (Mn), and sodium (Na) along with zinc (Zn) are vital elements needed in slight quantity for metabolic and redox functions [24]. They act as co-enzymes for catalytic enzymes in metabolic cell reactions, but increasing their concentration can lead to toxic condition and cause numerous carcinogenic effects [24, 25]. On the other heavy metals for instance aluminum (Al), lead (Pb), cadmium (Cd), gold (Au), mercury (Hg) and silver (Ag) do not have any biological role and are toxic to living organisms [24]. They are able to prevent the regular physiological and developmental functions of living organisms in minor amounts and responsible for a wide range of physiological diseases [24, 26, 27].

Heavy metals are of greater concern among the uncountable organic and inorganic compounds released into the aqueous environments due to their persistence, potential of bioaccumulation and toxicity in various species [24, 28].

They show pronounced toxicity effects in terms of bioaccumulation and biomagnification in tissues and food webs, respectively. Increases in heavy metal concentration, to levels higher than standard amounts identified, may lead to sub-lethal or even lethal impacts on aquatics and humans [24, 26, 28]. When heavy metals are taken up in higher concentrations, they are be responsible for posing serious health risks and can affect liver, brain, bone and lungs, although each metal has its own particular signs and symptoms [25, 26].

The key mechanism of heavy metal toxicity comprises the production of free radicals to cause oxidative stress, harm of biological molecules such as enzymes, proteins, lipids and nucleic acids, damage of DNA which is important to carcinogenesis besides neurotoxicity [24, 29]. Some heavy metal toxicity can be acute, while others can be chronic after long-term exposure which may lead to the damage of numerous tissues in the body for example the brain, lungs, liver and kidney causing diseases in the body (**Figure 3**) [30].

**Figure 3.** *Heavy metals: Sources, mechanism of action and its effects on humans.*

*Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

#### **3. Biological treatment**

For the reason that PAHs and HMs cause serious problems in environment even at little concentrations, elimination of these compounds has become an urgent obligation in recent decades, and it is essential to develop techniques for their removal [31, 32]. Many methods are being used for treatment of contaminated water environments. Pollutants can be removed using various treatment technologies, including chemical precipitation, oxidation or reduction, filtration, ion-exchange, reverse osmosis, membrane technology, evaporation and electrochemical treatment [33, 34]. However, these methods are always not effective. Moreover, they are expensive and relatively ineffective, and they can generate extra problems. Consequently, they are seen as unfavorable and uneconomical [35, 36].

In recent years natural treatment systems are regarded as the best available technology for treating various types of wastewaters. Nowadays experts have turned to a new method for removing pollutant from the environment using microorganisms [37, 38]. Removal of heavy metals and PAHs from aqueous solution by using microorganisms is called bioremediation which are considered to be the more appropriate than the physical and chemical methods because of their high removal and recovery efficiency, cost-effective and reducing the production of secondary toxic compounds [35].

Bioremediation is defined as the process whereby organic and inorganic wastes biologically become under controlled conditions to an innocuous state, or to levels below concentration limits established. Since the early 1900s, biological biomass used to diminish nutrients, pollutants and organic matters in wastewater [33, 35].

The mechanisms, such as biosorption, bioaccumulation and biodegradation, are involved in bioremediation. Both bioaccumulation and biosorption are the processes using which microbes or biomass gets bound to the HMs and pollutants from the surrounds and concentrates them [35, 36, 38].

Biosorption is a process in which microorganisms use their cellular structure to capture HM ions, which they then absorb onto the cell wall's binding sites. It is a passive uptake process and does not depend on the metabolic cycle [30]. Biosorption is a reversible and fast passive adsorption process, and there may be both living and dead biomass for biosorption [9, 38].

However, unlike biosorption, bioaccumulation by microbes is an active metabolic process in which heavy metals accumulate and are transported into intracellular living bacterial cells using proteins. Endocytosis, ion channels, carrier-mediated transport, complex permeation and lipid permeation are all involved in HM bioaccumulation in the bacterial membrane [39]. This process depends on microorganism cell metabolism. In contrast to biosorption where dead biomass cells are still able to eliminate HMs, bioaccumulation occurs only by living biomass cells [40].

In biodegradation, microorganisms degrade toxic organic pollutants into safe and non-toxic compounds. In fact, biodegradation basically occurs due the actions of multiple organisms which enzymatically deal with the pollutants and turn them into innocuous products [41, 42].

Using biological techniques for eliminating of heavy metals and aromatic compounds from marine ecosystems is considered reasonable. There are number of advantages associated with the use of microorganisms to removal of pollutants (**Figure 4**) [43, 44].

Bacteria, microalgae, fungi and yeast are the most important microorganisms that are commonly used for bioremediation [45–47]. They are extensively dispersed on the environment because of their significant metabolic capacity and they can simply


**Figure 4.** *Types of bioremediation mechanisms and their benefits.*

grow in a wide range of environmental conditions [43]. However, compared to other microorganisms, bacteria signified greater removal ability due to their small size, high rate of growth and reproduction and active biosorption sites such as peptidoglycan. On the other hand, bacteria are considered the most exceptional bio-sorbents among all other organisms because of their high surface-to-volume ratios and active sites of chemosorption in their cell wall, such as teichoic acid [48, 49].

#### **4. Persian gulf**

Around 70% of the earth is enclosed by sea water. Oceans provide food, recreation and transportation that sustain a significant portion of the world's economy [50]. The Persian Gulf is one of the most diverse water environments in the world [51]. There are various types of marine creatures including corals, sponges and fish in this marine environment [52, 53]. Mangrove forests are found in this aquatic ecosystem. In mangrove forests, some of the complex ecological relations between organisms living in intertidal zones [54]. Other marine creatures in the Persian Gulf are also very diverse. In recent years, because of human activities, various contaminants have entered the oceans and marine environments, leading to the change of life in these main aquatic ecosystems [55, 56]. The Persian Gulf is one of the main ways of transferring energy and goods. Since about 60% of the world's oil is transported to the Persian Gulf, oil pollution is unavoidable [57, 58].

In the countries of the Persian Gulf, air, soil and water pollution by mineral and organic pollutants are an important subject. Also, during the last 30 years, there have been three wars in the Persian Gulf: The Islamic Republic of Iran and Iraq War (1980–1988), the first and second Persian Gulf Wars (1991 and 2003, respectively) [59]. Thus, in 1991, a large oil spill occurred in the Persian Gulf, and as a consequence, 6 to 8 million barrels of Kuwaiti crude oil were discharged into the Persian Gulf [60]. The oil spill due to the first Persian Gulf War is considered the worst oil spill in history. Therefore, a large amount of research was focused on the same spill, which

*Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

#### **Figure 5.**

*Main environmentally sensitive parts of the Persian Gulf, key oil and gas infrastructures, chief ports, desalination plants and nuclear energy facilities [57].*

confirmed the range of influence of the oil spill of 400 km from the point where the spill occurred to the coastlines of Saudi Arabia [3, 59, 60]. Moreover, numerous spills produced by routine oil operations and tankers. So, The Persian Gulf has experienced numerous and enormous pollution [61]. On the other hand, reducing the distribution and dispersal of pollutants because of the shallow depth and limited contact of the Persian Gulf with other aquatic ecosystems causes contaminants to remain in the Persian Gulf for a long time [62, 63].

These factors have turned the Persian Gulf into one of the most polluted seas in the world. Oil pollution in the Persian Gulf has not been managed, many corals, sponges. Mangrove forests are soon destroyed, and biodiversity is significantly reduced. Therefore, the protection of this water environment is more vital in the world (**Figure 5**) [63–65].

Many studies have been conducted to remove heavy metals and PAHs from aquatic environment using biological adsorbents, which are considered the most appropriate methods compared to other methods [66, 67]. Overall, various species of bacteria have been isolated and reported by numerous researchers in the Persian Gulf, maybe because of its high resistance to an extensive range of oil hydrocarbons and heavy metals [3, 6, 68]. According to mentioned abilities of bacteria, many writers have suggested the use of this method in removing oil pollution and heavy metals in aquatic environments such as the Persian Gulf [69–74].

In this chapter, we decided to have a review of the studies done on isolation and identification of indigenous bacteria and evaluation of its ability in removal of heavy metals and polycyclic aromatic hydrocarbons in Persian Gulf.

#### **5. A review of studies on bioremediation in the Persian Gulf**

Marine ecosystems around the world, such as the Persian Gulf, are suitable habitats for all kinds of native bacteria [75]. These bacteria belong to different genera that are mostly found in the aerobic zone of marine sediments [71, 76]. In the last two decades, many researches have been conducted on non-symbiotic bacteria and their performance in cleaning the Persian Gulf [3, 6, 77–81].

Numerous hydrocarbon-utilizing bacteria have been isolated from the Persian Gulf which Proteobacteria, for example, Gammaproteobacterial genera (e.g., Acinetobacter, Macrobacteria and Alcanivorax), Alphaproteobacterial genera (e.g., Tissrella and Zavarzina) and also Actinobacteria are the dominant cultivatable marine bacteria [82–84].

Studies have shown that marine bacteria often belong to the genera of Marinobacter, Microbacterium, Rhodococcus, Kocuria, Alcanivorax, Microbacterium, Pseudomonas, Pseudoalteromonas, Dietzia and approximately all of them are found in the aerobic zone of marine sediments. Besides the bacteria referred above, Heretofore, various hydrocarbon-degrading bacteria have been caught from Kish Island in Iran. The most commonly reported genera of hydrocarbon-degraders include Pseudomonas, Acinetobacter, Nocardia, Vibrio and Achromobacter.78 s [78, 85–88].

Likewise, Hassanshahian et al. separated bacteria resistant to various petroleum compounds from the Persian Gulf. In their research, they succeeded in isolating 25 oil-resistant bacteria from the sediments of the Persian Gulf and the Caspian Sea. Molecular identification showed that these bacteria belong to these genera: Acinetobacter, Cobetia, Gordonia, Rhodococcus, Pseudomonas, Halomonas, Microbacterium, Marinobacter and Alcanivorax. Their results showed that the studied bacteria can be used to remove pollutants from the environment and reduce the level of oil pollution in the Persian Gulf and the Caspian Sea [89].

In the other study, *Rhodococcus ruber* KE1 was isolated from Persian Gulf water and sediment (khark Island, south part of Iran), and the ability of this bacterium to break down petroleum compounds was evaluated. Different experimental parameters such as pH, temperature, crude oil concentration and agitation speed were optimized to achieve the maximum degradation efficiency. The best results were measured at pH 8.5, temperature 40°C, stirring speed 250 rpm and crude oil concentration 1% (v/v). Associated data showed that *R. ruber* KE1 under optimal conditions is able to remove about 90% of the total hydrocarbons after one week. The measurement of residual nitrogen and sulfur showed a decrease of 48 and 44%, respectively. The ability of this particular strain as a surfactant producer was measured under optimal conditions. A decrease in surface tension was recorded from 60 (control) mN/m to 26 mN/m [90].

In the study of Kafilzadeh et al., sampling of mangrove sediments was done. After bacterial counting and enrichment in MSM medium, the isolated bacteria were purified on blood agar. Bacteria were identified by different biochemical tests and PCR. *Brevibacterium iodinum*, *Acinetobacter calcoaceticus*, *Corynebacterium variabile*, Enterobacter sp. and Acinetobacter lowffi were isolated from mangrove sediments. Consequences displayed 86.2, 81.4, 75.2, 57.3 and %55.8 of substrate was degraded by these bacteria respectively. Based on results of growth studies, *B. iodinum*, *A. calcoaceticus* and *C. variabile* showed the maximum growth after 72 hours, and Enterobacter sp. and Acinetobacter lowffi had the maximum growth after 84 hours of incubation [91].

However, based on other studies conducted in the northern coasts of the Persian Gulf, more different species of bacteria resistant to heavy metals and petroleum hydrocarbons were found [6, 77, 92–95]. One of the most important bacterial species isolated from the sediments of the Persian Gulf is the species belonging to the genus Pseudomonas [77, 92–95].

*Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

Among ten bacterial species isolated from marine sediment, by Safahieh et al., one strain represented high potential to grow in medium supplemented with copper and phenanthrene. Isolated bacterium was identified as Pseudomonas sp. by biochemical tests. Over 70% of copper absorbed on Pseudomonas sp. within 150 min. In addition, about 96.52% of primary concentration of phenanthrene was degraded during 120 h. Based on the capacity of isolate in degradation of phenanthrene and biosorption of copper, this species is introduced as a suitable microorganism for bioremediation of polluted environments [77].

Also, Lamoochi et al., in another study, *Pseudomonas aeroginosa* was isolated and identified as a resistant bacterium to zinc from Musa Bay sediments (located in the North of the Persian Gulf, Iran). Investigating the growth of *P. aeroginosa* bacteria in an aqueous solution containing 20, 40, 80, 160 and 320 mg/L of zinc showed that increasing the concentration of zinc produced a decrease in bacterial growth. The maximum bacterial growth of 0.93 was achieved at a concentration of 20 mg/L zinc. By increasing the zinc concentration to 320 mg/L, bacterial growth reduced to 0.37, which showed an important difference with the maximum bacterial growth at 20 mg/L zinc concentration. *P. aeroginosa* can remove 86% of Zn at a concentration of 25 mg/L Zn [92].

In order to compare the growth and ability of biosurfactant production in bacteria present in oil-contaminated sediments of the Persian Gulf (Khor Musa), samples were taken from the contaminated sediments of the region. Two species of bacteria Psedomonas stutzeri and *Alcaligenes denitrificans* were isolated and purified from oil contaminated sediments and identified as oil-resistant bacteria through morphological and biochemical tests. Bacterial growth was measured by a spectrophotometer at optical density at a wavelength of 600. Evaluation of biosurfactant was done with blood agar, drop collapse and oil spread methods. Psedomonas stutzeri showed that it is able to produce biosurfactant. According to results, Psedomonas stutzeri has a good growth in the media comprising Antheracene as single source of carbon and energy. Furthermore, the data showed that the growth of biosurfactantproducing bacteria (Psedomonas stutzeri) was better than *Alcaligenes denitrificans* due to the increased solubility of anthracene and its increased bioavailability in the environment [93].

Uptake of heavy metal ions by *Pseudomonas aeruginosa* strain MCCB 102 isolated from the Persian Gulf was investigated in two single and multi-mix forms. The highest adsorption was observed for Cu, Zn, Cd and Pb, respectively. Removal of metals was maximized when the metal ions were in a single form. Scanning electron microscope (SEM) analysis showed *P. aeruginosa* strain MCCB 102 accumulated heavy metals in the cell wall and along the external cell surfaces [96].

A study by Shahaliyan et al. (2016) aimed to isolate and identify the species *Ochrobactrum anthropi* and *Pseudomonas putida* as indicators for measuring lead absorption and degradation of anthracene in laboratory conditions. The consequences presented that the mentioned species could grow well in 50 mg/l of lead and 30 mg/l of anthracene. The maximum growth at concentrations of 50 mg/l of lead and 30 mg/l of anthracene was measured 1.39 and 0.530, respectively. The results of the study of the capability of lead uptake by *O. anthropi* at a concentration of 50 mg/l and anthracene elimination by P. putida at a concentration of 30 mg/l indicated that the mentioned bacteria started absorbing lead and anthracene at the time of inoculation and rapidly reduced their concentrations in the solution. Elimination of lead and anthracene by *O. anthropi* and *P. putida* from the metal and hydrocarbon solutions continued actively till the last moments of measurement and at the end of the experiment, 84% of lead and 77.986% of anthracene were removed [95].

Pseudomonas Sp. is a saprotrophic bacterium with adaptability to various environments [77, 96, 97]. This bacterial species has diverse aerobic metabolisms for bioremediation of aromatic compounds and biosorption of heavy metals. It appeared that it has the ability to use benzene, toluene and naphthalene as the sole source of carbon and energy. The ability of Pseudomonas species in degradation of hydrocarbon and heavy metal materials has been reported by many researchers [98, 99].

Also, various species of Bacillus have been isolated and reported by several investigators possibly due to its high resistance to wide range of oil hydrocarbons and heavy metals According to previous studies, the genus Bacillus has a significant ability to remove heavy metals and PAHs [6, 100–103]. This genus comprises gram-positive, aerobic and spore-producing bacteria with the ability to absorb heavy metals due to special binding sites in their cell walls (such as teichoic and teichronic acids) [6, 104–106].

In another study, native bacteria resistant to lead were isolated from the surface sediments of Imam Khomeini Port (Persian Gulf). The isolated bacterium *Bacillus* 


#### **Table 1.**

*Bacteria removing oil pollutions separated from the Persian Gulf.*

#### *Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

*firmus* was identified through biochemical tests. Examining the growth of *B. firmus* in concentrations of 50, 100, 200, 400 and 800 mg/liter showed that the maximum growth of bacteria is in the concentration of 50 mg/liter of lead. This bacterium was also able to grow well in high concentrations of lead (800 mg/L), which indicates the high resistance of the bacterium to this metal. Examining the results of the ability of *B. firmus* bacteria to bioabsorb lead at concentrations of 50, 100 and 200 mg/liter showed that this bacterium is able to remove 95% of lead from the metal solution [103].

Based on the studies of Lamouchi et al., Bacillus pastorii and *Amphibacillus xylanus* bacteria were isolated, purified and identified from the oil-contaminated sediments of Imam Khomeini Port. The mentioned bacteria grew well in culture medium containing 30 ppm anthracene. The results showed that compared to *A. xylanus*, Bacillus pastori grows and adapts quicker in the culture medium containing anthracene hydrocarbon at a temperature of 30°C [107].

A study conducted by Salamat et al., *Bacillus subtilis* resistant to anthracene and lead was isolated from the polluted sediments of the Persian Gulf. Biosurfactant production was investigated using three methods: drop collapse, blood agar and oil spreading. The maximum growth of bacteria in 30 mg/l anthracene and 50 mg/l lead was recorded by spectrophotometer. A significant proportion of anthracene (69.95%) was reduced after 120 hours, and the maximum percentage of lead absorption (82%) was observed after 150 minutes. The consequences showed that the separated bacteria are able to eliminate anthracene and lead [6].

The high capacity of the Bacillus bacterium probably owing to the species diversity in the environment and its spores which protected the bacteria from intense environmental conditions [6]. Organic compounds are considered as a nutritional source for bacteria. Specific sensors activated in the bacteria in medium comprising hydrocarbons, enabled them to bind to these organic compounds and emulsify and move them into their body [6, 106].


The results of the study by Abyar et al. showed that among different separated bacterial species (Pseudomonas, Bacillus, Alcaligenes and Geobacillus),

#### **Table 2.**

*Heavy metal removing bacteria isolated from sediments.*

*Achromobacter denitrificans* strain PQ-1 was the most resistant bacteria against cadmium. Consequences also indicated that metal biosorption by *A. denitrificans* strain PQ-1 is accomplished of eliminating 55.1%, 50.7% and 43.5% of the cadmium from 25, 50, and 100 mg/l concentrations, respectively [108].

*Micrococcus luteus* as a zinc-resistant bacterium was isolated from Persian Gulf sediments and identified using biochemical tests and bacteriological sources. The bacteria grew well in high concentration of zinc (800 mg/liter). The results showed that the removal of zinc increases with the increase of zinc concentration, so that the highest amount of removal (169 ± 0.4 mg/L) at the concentration of 200 mg/L of zinc and the highest percentage of bioabsorption of zinc (76%) at the concentration of 50 mg/L occurred after 150 min of incubation. The results showed that *M. luteus* is resistant to changes in the percentage of salt in the environment and can grow in a wide range of salt concentration (**Tables 1** and **2**) [80].

## **6. Conclusion and future perspective**

While environmental biotechnology is approximately based on a variety of methods of environmental protection and restoration of damaged ecosystems, for a decade it has been mostly associated with bioremediation, rehabilitation, and waste treatment technology. Most of the Persian Gulf regions, especially the coastal areas, have been contaminated with oil and heavy metals during the recent Persian Gulf War (1990) and sea transportation due to the presence of many industries. Microorganisms can degrade organic and inorganic pollutants as a source of carbon and energy, and this may pave the way for the use of remediation and cleanup methods for sediments contaminated with oil and heavy metals. There are several problems related to the environment contaminated with oil and heavy metals that affect human health and the quality of the environment. The present study may provide opportunities for biological remediation of areas contaminated with various pollutants for future studies in the Persian Gulf region.

### **Author details**

Razieh Lamoochi1 \* and Kobra Jalali2

1 Department of Marine Biology, Marin Biology, Marine Science and Technology University of Khorramshahr, Iran

2 Khorramshahr Marine Science and Technology University, Iran

\*Address all correspondence to: raziehlamoochi@yahoo.com

© 2023 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

*Investigating Bacterial Communities Resistant to Heavy Metal and PAHs Pollutants in the Persian… DOI: http://dx.doi.org/10.5772/intechopen.110265*

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