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Biological Journal of Microorganism th 8 Year, Vol. 8, No. 32, Winter 2020 Received: November 18, 2018/ Accepted: May 21, 2019. Page: 15-231- 8

Microbial Diversity of Non-flooded High Temperature Petroleum Reservoir in South of Iran

Mohsen Pournia Department of Microbiology, Shiraz Branch, Islamic Azad University, Shiraz, Iran, [email protected] Nima Bahador * Department of Microbiology, Shiraz Branch, Islamic Azad University, Shiraz, Iran, [email protected] Meisam Tabatabaei Biofuel Research Team (BRTeam), Karaj, Iran, [email protected] Reza Azarbayjani Molecular bank, Iranian Biological Resource Center, ACECR, Karaj, Iran, [email protected] Ghassem Hosseni Salekdeh Department of Biology, Agricultural Biotechnology Research Institute, Karaj, Iran, [email protected]

Abstract Introduction: Although and are able to grow and adapted to the petrol reservoirs during several years, there are no results from microbial diversity of oilfields with high temperature in Iran. Hence, the present study tried to identify microbial community in non-water flooding Zeilaei (ZZ) oil reservoir. Materials and methods: In this study, for the first time, non-water flooded high temperature Zeilaei oilfield was analyzed for its microbial community based on next generation sequencing of 16S rRNA genes. Results: The results obtained from this study indicated that the most abundant bacterial community belonged to phylum of ( ) and , while other phyla ( , and ) were much less abundant. subtilis , B. licheniformis , Petrotoga mobilis , P. miotherma, Fervidobacterium pennivorans , and Thermotoga subterranea were observed with high frequency. In addition, the most abundant archaea were Methanothermobacter thermautotrophicus . Discussion and conclusion: Although there are many reports on the microbial community of oil filed reservoirs, this is the first report of large quantities of Bacillus spp. from a high temperature oil reservoir. Key words: Microbial Diversity, 16S rRNA, Next Generation Sequencing, Non-Water Flooded, High Temperature Oilfield

*Corresponding Author Copyright © 2020, University of Isfahan. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/BY-NC-ND/4.0/), which permits others to download this work and share it with others as long as they credit it, but they cannot change it in any way or use it commercially.

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Introduction contaminant microorganisms that are The severe conditions within the oil capable to colonize the upper cooler parts reservoir make it possible for certain of the oil well (9-11). Contamination of microorganisms to adapt to these oilfields happens during drilling, sampling conditions. These bacteria have been and enhanced oil recovery (EOR), adapted to reservoirs conditions during especially during the water flooding many years. Various groups of processes (1, 9, 11, 12). It is difficult to microorganisms isolated from oil distinguish indigenous microorganisms reservoirs with diverse physiological and from allochthonous ones in these oil metabolic characteristics and phylogenetic reservoirs. affiliations including sulfate reducing In this study, for the first time, the bacteria (SRB), fermentative bacteria, microbial diversity of a non-water nitrate or manganese and iron reducers, flooding oilfield with high temperature in sulphidogens, acetogens and methanogens. southern Iran was evaluated using next These microorganisms influence the generation sequencing of 16S rRNA gene quality of crude oil and reservoir analysis. conditions during metabolism activities (1- 3). Therefore, in recent years, many Materials and Methods studies have been carried out to identify Reservoir Conditions: All inoculum varieties of microbial populations sources originated from non-water inhabiting oil reservoirs around the world flooding Zilaei (ZZ) oil reservoir which is (4). High-temperature oilfields are always located at the northeastern of Ahwaz, Iran, considered more than other oil fields (5-8), with a length of 3 km and a width of 8 km. for extending new technologies, microbial According to internal report of National enhanced oil and energy recovery, control Iranian South Oil Company (NISOC, of souring, bioremediation and further 2014), the study area was carbonate oil understanding of biogeochemical bed, having the salinity of 194000 ppm, procedures and life in extreme with bottom-hole temperature of 85 - 90 environments (9). °C, at a depth of approximately 3700 m By molecular techniques and non- above sea level. The reservoir contained dependent culturing methods, a much light crude oil, holding an API gravity of larger range of different thermophilic 37 °C and pH of 8.0 (13). microorganisms were detected from high Sampling : Five liters ZZ produced temperature oilfields. Most of Archaea water sample were obtained from its oil- belong to CO 2-reducing methanogens water processing site, during the period of including Methanobacteria , Methanococci July to December 2016. The bottles were and Thermococcales and Bacterial filled completely and immediately taken to sequences affiliated with Firmicutes and the laboratory for extraction of DNA (14). Thermotoga in high-temperature oil DNA Extraction: All samples were reservoirs (2, 5-8). Nevertheless, some filtered directly using 0.2-µm Startolab moderate and non-thermophilic 150 V filter (Sartorius Biotech) and placed microorganisms were identified in various in 5 ml Homogenizer buffer (100 mM quantities in these oilfields. It has been Tris–HCl (pH 8.2); 100 mM EDTA (pH hypothesized that the mesophilic 8); 1.5 M NaCl). The mixture was microorganisms may originate from incubated under shaking conditions (150

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Archive of SID Microbial Diversity of Non-flooded High Temperature Petroleum Reservoir in South of Iran 17

rpm) for 12 h at room temperature for re- performed by pyrosequencing the suspended microbial cells. The amplified 457 bp of the 16S rRNA metagenomic DNA extraction was gene amplifying by the 349F: 5'- performed in a harsh manner which GYGCASCAGKCGMGAAW -3' and combined several lysis methods together. 806R: 5'- For achieving better result in DNA GGACTACVSGGGTATCTAAT -3' extraction, the treatment of the glass bead primers with PCR reaction conditions as was used along with lysis buffer. The lysis same as above (14, 16). The PCR buffer was formulated according to the incubation for bacterial and archaeal method developed by Siddhapura et al. amplicon libraries products was performed (15). The re-suspended microbial cells according to Pournia and colleagues (14). were applied to the enzymatic buffer (Tris- PCR products were purified and quantified HCl pH 8; 20 mM, EDTA pH 8; 10 mM by the Qubit flourometer (Invitorgen, and Triton X-100 1.2%) with 20 mg/ml USA). The amplicon pool was used for lysozyme and incubated overnight under pyrosequencing on a GS Junior platform shaking conditions. Before the addition of (454 Life Sciences, Roche, Macrogen) lysis buffer, the tubes were vigorously according to the manufacturer’s mixed with 1g glass beads by a vortex and instructions using Titanium chemistry. subjected to intermittent freeze thaw in the Bioinformatics Analysis: Raw reads liquid N 2 treatment. The next steps for the were firstly filtered according to the 454 chemical lysis and purification were amplicon processing pipeline. Sequences continued according to Siddhapura et al were investigated by QIIME 1.6.0 (15). The concentrations of double- software (17). Raw reads were stranded DNA in the extracts were demultiplexed and further filtered through determined using the Quant-iT dsDNA the split library of QIIME. For 16S rRNA Assay Kit and the Qubit fluorometer gene reads and the analysis were carried (Invitrogen, USA) . out as follows: sequences that passed the 16S rRNA Gene Amplicon Library and quality filter were denoised and singletons High-throughput Sequencing: The bacterial were excluded. OTUs defined by a 97% of diversity was studied by pyrosequencing similarity were picked using the uclust the amplified V1–V3 domain of the 16S method and the representative sequences, rRNA gene amplifying a fragment of 520 selected as the most abundant in each bp by the 27F: 5'- cluster, were subjected to the RDPII AGAGTTTGATCCTGGCTCAG -3' and classifier to get the assignment 534R: 5'- ATTACCGCGGCTGCTGG -3' and the relative abundance of each OTU primers (14). Ligated 454-adaptors were using the Greengenes database (17). included in the forward primer, followed by a 10 bp Multiplex Identifier (MID). Results PCR amplification was done by 1X Rarefaction Curve: In this research, enzyme buffer, 0.2 mM dNTPs mixture 6.88 µg archeal and 22.3 µg bacterial DNA (Fermentas), 1 U High-Fidelity DNA per µL of the PCR product were obtained Polymerase (Fermentas), 0.5 µM of each from the produced water of Zilaei oil field. primers (forward and reverse), 1.5 mM During their sequencing, 6350 archeal and MgCl 2 and 2 µL of the DNA sample. The 14100 bacterial sequences were identified. archaeal community analysis was The rarefaction curve is shown in Figure 1.

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Archive of SID 18 Biological Journal of Microorganism, 8th Year, Vol. 8, No. 32, Winter 2020

Bacteria Archaea

100 90 80 70 60 50 40 30 Observed Observed 20 10 0 0 5000 10000 15000

Number of Read

Fig. 1- Rarefaction Analysis of 16S rRNA Archaea and Bacteria Genes

Archaeal Community in Crude Oil: The was observed with the frequency of 26.6% 16S rRNA sequencing of archaeal genes while Methanothermobacter thermophilus , showed that there are 7 different archeal Methanotorris formicicus , Methanococcus species which belonged to the phylum of aeolicus , carlsbadense , and one uncultured Haloplanus natans and archaeon (Fig. 2). The family of oshimae were characterized by less than Methanobacteriaceae , species of 1% predominance (Table 1). Methanothermobacter thermautotrophicus

Table 1- Phylogenetic Affiliations and Relative Abundance of Archaeal Clone Library Frequency Archaea/ Domain: Class Family / Species (%Coverage) Archaea / Unclassified Unclassified; Uncultured archaeon 0.62 Euryarchaeota: Halobacteria ; Haloplanus natans 0.62 Euryarchaeota; Halobacteria Halobacteriaceae ; Halosimplex carlsbadense 0.62 Euryarchaeota; Methanococci Methanococcaceae ; Methanococcus aeolicus 0.62 Euryarchaeota; Methanococci Methanocaldococcaceae ; Methanotorris formicicus 0.62 Euryarchaeota; Methanobacteria Methanobacteriaceae ; Methanothermobacter thermautotrophicus 26.66 Euryarchaeota; Methanobacteria Methanobacteriaceae ; Methanothermobacter thermophilus 0.62 Euryarchaeota; Picrophilaceae ; 0.62

Bacterial Community in Crude Oil: that the major group of bacteria belonged Phylogenetic association of bacterial 16S to the family of Bacillaceae , genera of B. rRNA genes sequences regain from ZZ subtilis and B. licheniformis . While other produced water oilfield included members main bacterial groups included the family of Firmicutes ; Bacilli (41.63%), of Thermotogaceae , genera of Petrotoga (24.69%), Firmicutes ; mobilis , Fervidobacterium pennivorans , Clostridia (0.53%), Proteobacteria Petrotoga miotherma and Thermotoga (0.43%), Actinobacteria (0.1%), subterranea were observed. In addition, Synergistetes (0.04%), one unclassified genus has been identified (0.02%), and unclassified Bacteria, MPZ with the frequency of 1.56%. The other 101 (1.56%) as shown in Figure 2. recognized bacteria in this oil field were Sequence alignment studies showed abundantly less than 0.5% (Table 2).

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Bacteria Bacteria (Unclassified); 1.56% Proteobacteria (Unclassified); 0.02% Proteobacteria (Alphaproteobacteria); 0.35% Proteobacteria (Betaproteobacteria); 0.02% Proteobacteria (Gammaproteobacteria); 0.04% Synergistetes (Synergistia); 0.04% Actinobacteria (Actinobacteria); 0.1% Firmicutes (Bacilli); 41.63% Firmicutes (Clostridia); 0.53% Thermotogae (Thermotogae); 24.69% Bacteroidetes (Bacteroidia); 0.02% Archaea Archaea (Unclassified); 0.62% Euryarchaeota (Halobacteria); 1.24% Euryarchaeota (Methanococci); 1.2% Euryarchaeota (Methanobacteria); 27.28% Euryarchaeota (Thermoplasmata); 0.62% Fig. 2- Relative Abundance of Bacterial and Archaeal Groups within Clone Libraries

Discussion and Conclusion to identify methanogens in Iranian oilfields. Archaeal sequences with a close However, Pournia et al. (14) by molecular relationship to the family members of methods identified several different Methanobacteriaceae , genus of methanogens from two non-water flooded Methanothermobacter , had the greatest oil reservoirs (LA and HK, located south of frequency in the samples taken from the ZZ Iran) with an average temperature of 54 and reservoir (Table 1). The M. 45 °C, respectively. The genus thermautotrophicus is a thermophilic, Methanofollis was observed with high chemoautotroph, non-motive, obligatory presence, while genera of anaerobic, which consumes H 2/CO 2 for Methanothermobacter , methanogenesis (18). This methanogens Methanobrevibacter, and other species of Methanothermobacter Methanomethylovorans and have been reported many times from Methanothermococcus were characterized various oilfields at different temperatures with a lower abundance. by Orphan in South Elwood oil field, The major group of bacteria belonged to California (7), in Linch, Kalol and the division of Firmicutes (Bacilli ) and Nandasan oil wells, India (19), high Thermotogae (Fig. 2). Phylum of temperature shengli oil reservoir, China Firmicutes and Thermotogae are commonly (20-22), high temperature not water flooded more abundant taxa in non-water flooded Niburi oil field in Japan (23), high- oilfield, while in the flooded oil reservoirs, temperature horizons of the Dagang and Proteobacteria is usually seen Kongdian oilfields, China (24-26), high predominantly (7, 9, 23, 29). However, in temperature gas-water producing Niigata this reservoir, only B. subtilis and B. wells, Japan (27) and high temperature, licheniformis belonged to the phylum of water-flooded Huabei Petroleum (28). Firmicutes which was present in large Resource studies show that no quantities, and the rest are much less comprehensive study has been carried out abundant.

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Table 2- Phylogenetic Affiliations and Relative Abundance of Bacterial Clone Library Frequency Bacteria/ Domain; Class Family; Genus Species (%Coverage ) Bacteria / Unclassified Unclassified; Uncultured bacterium (MPZ 101) 1.56 Proteobacteria; Unclassified Unclassified; Uncultured proteobacterium 0.02 Proteobacteria; Alphaproteobacteria Unclassified; Uncultured alphaproteobacterium 0.06 Proteobacteria; Alphaproteobacteria Sphingomonadaceae ; Sphingomonas sp. EK-1 0.24 Proteobacteria; Alphaproteobacteria Rhizobiaceae ; Sinorhizobium sp. R-25067 0.02 Proteobacteria; Alphaproteobacteria Methylobacteriaceae ; Methylobacterium rhodesianum 0.03 Proteobacteria; Betaproteobacteria Unclassified; Uncultured betaproteobacterium 0.02 Proteobacteria; Gammaproteobacteria Enterobacteriaceae ; Enterobacter aerogenes, E. cloacae 0.04 Synergistetes; Synergistia Synergistaceae ; Aminobacterium colombiense 0.02 Synergistetes; Unclassified Unclassified; Synergistetes bacterium SGP1 0.02 Actinobacteria; Actinobacteria Propionibacteriaceae ; Propionibacterium acnes 0.06 Actinobacteria; Actinobacteria Actinomycetaceae ; Actinomyces viscosus 0.02 Actinobacteria; Actinobacteria Corynebacteriaceae ; Corynebacterium matruchotii 0.02 Firmicutes; Bacilli Bacillaceae ; 35.53 Firmicutes; Bacilli Bacillaceae ; 4.42 Firmicutes; Bacilli Bacillaceae ; Bacillus sp. (MPZ 103) 0.45 Bacillaceae ; Bacillus amyloliquefaciens, B. thermoamylovorans, B. pumilus, B. mojavensis, B. methanolicus, B. weihenstephanensis, B. Firmicutes; Bacilli 0.63 hwajinpoensis, B. vallismortis, B. clausii, B. sp. 3EC2B1, B. sp. KHg1, B. sp. RH219 Firmicutes; Bacilli Bacillaceae ; necropolis 0.02 Firmicutes; Bacilli Bacillaceae ; karajensis, H. trueperi 0.04 Firmicutes; Bacilli Paenibacillaceae ; Paenibacillus polymyxa 0.02 Firmicutes; Bacilli ; sacchari 0.02 Firmicutes; Bacilli Staphylococcaceae ; Staphylococcus epidermidis 0.18 Firmicutes; Bacilli Streptococcaceae Lactococcus lactis 0.2 Firmicutes; Bacilli Lactobacillaceae ; Lactobacillus curvatus, L. sp. (MPZ 102) 0.06 Streptococcaceae ; Streptococcus parauberis, St. gordonii, St. Firmicutes; Bacilli 0.06 gallolyticus Firmicutes; Clostridia Clostridiaceae ; Clostridium sp. Kas107-2, Cl. sp. MK11 0.24 Firmicutes; Clostridia Lachnospiraceae ; Butyrivibrio fibrisolvens 0.23 Firmicutes; Clostridia Peptococcaceae ; Desulfosporosinus sp. DB 0.02 Firmicutes; Clostridia Thermoanaerobacteraceae ; Moorella thermoacetica 0.02 Firmicutes: Clostridia Ruminococcaceae ; Ruminococcus albus 0.02 Thermotogae; Thermotogae Thermotogaceae ; Fervidobacterium pennivorans 5.25 Thermotogae; Thermotogae Thermotogaceae ; Thermotoga subterranea 2.84 Thermotogae; Thermotogae Thermotogaceae ; Petrotoga mobilis 14.05 Thermotogae; Thermotogae Thermotogaceae ; Petrotoga miotherma 2.55 Bacteroidetes; Bacteroidia Porphyromonadaceae ; Tannerella forsythia 0.02

A variety of species related to the genus (34) recovered Bacillus sp. (B. cereus and of Bacillus have been recognized from B. licheniformis ) from core samples of a different oil reservoirs such as in high- high temperature Virgin oil reservoir temperature water-flooded reservoir, China (Brazil) and suggested that these bacteria (5), Caratinga and Barracuda high were autochthonous in such environments. temperature oil fields in the Rio de Janeiro It seems that the existence of the spore and (10), in the LA and HA oilfields, Iran (14), use of other compounds like nitrate as the oily sludge and petroleum muck, India (30, final receptor of the electron during 31), high temperature Shengli oilfield, respiration, help them to survive in harsh China (32), and Potiguar oilfield, Brazil conditions and penetrate deeply into (33). Furthermore, Cunha and colleagues petroleum reservoirs (35). This genus was

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biotechnologically useful through much oilfield, Thermotogae (Petrotoga ), diversified metabolic pathway. Potentials of Firmicutes (Bacillus ) and Synergistes production of some alcohols, organic acids, (Thermovirga ) were more abundant. gas, biopolymer and biosurfactants make Nevertheless, microbial diversity of long- them the ideal bacteria to be used in duration gas injection HK oil reservoir, bioremediation of oil pollution and the were Synergistetes (Anaerobaculum ), MEOR technology (13, 32, 35). To the best Proteobacteria (Rhodocyclaceae ) and of authors’ knowledge, Bacillus sp. has not Firmicutes (Bacillus ), respectively (14). been reported in large quantities from high However, in two water flooded oil fields in temperature oil reservoirs. Oman, Middle East (hole temperature is In contrast, several genera of the phylum about 64 °C), the major bacteria identified of Thermotoga have been reported belonged to the Thermotogae , frequently from heated geothermal Proteobacteria and Firmicutes (40). It environments and different high seems that EOR processes increase the temperature oilfields (36). Thermotogaceae microbial diversity and the frequency of currently comprises of the genera, Proteobacteria and Synergistetes , in these Thermotoga , Thermosipho , adjoining oilfields (14). Fervidobacterium , Geotoga , Petrotoga , Marinitoga , Kosmotoga , Thermococcoides Acknowledgements and Oceanotoga (36). All members have a We would like to thank Bijan Noaparast characteristic outer sheath like structure (Masjed Soleyman oil and gas Production (toga) and some species are able to reduce Company) for technical adviser. This work sulfur compounds and produce H 2S (36, was supported by National Iranian South 37). The Petrotoga species have been Oil Company (NISOC), Khuzestan, Iran. reported only in oil reservoirs, but Furthermore, the authors are thankful from Fervidobacterium and Thermotoga are also research department of Shiraz, Islamic isolated from the hot springs. Grassia et al. Azad University for accepting the PhD (38) isolated two bacteria that resembled F. project in this regard. nodosum from high temperature oil fields in Venezuela and Australia. The F. References pennivorans was isolated from a hot (1) Varjania SJ., Gnansounoub E. Microbial springs in Portugal (36, 37, 39). However, dynamics in petroleum oilfields and their to the best of authors’ knowledge, this is relationship with physiological properties of the first report of the F. pennivorans from petroleum oil reservoirs. Bioresource an oil field. Technology 2017; 245: 1258–1265. The abundance of other bacteria in this (2) Ollivier B., Magot M. Petroleum Microbiology . oil field was very low (less than 0.5%). It Washington DC: ASM Press; 2005. seems that lack of water flooding, high (3) Magot M., Ollivier B., Patel BKC. Microbiology temperatures and salinity have caused of petroleum reservoirs. Antonie van Leeuwenhoek relatively limited microbial diversity. The 2000; 77: 103–116. frequency of Proteobacteria was only (4) Liu H., Yao J., Yuan Z., Chen H., Wang F., Masakorala K., Choi MMF. Degradation of about 0.43%, while these bacteria are often hydrocarbons by indigenous microbial more abundant in flooded high-temperature communities from two adjacent oil production oil fields (7, 9, 23, 29). wells in one block. Energy Sources, part A: Comparing the results with its adjacent Recovery, Utilization and Environmental Effects oilfields in southern Iran (LA and HK) 2016; 38 (23): 3423–3434. showed that in the non-water flooded LA (5) Li H., Yang SZ., Mu BZ., Rong ZF., Zhang J. Molecular phylogenetic diversity of the

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[email protected] : * [email protected] : meisam_ [email protected] : [email protected] :

: . . . ( ZZ )

: . S rRNA 16

: Proteobacteria , Actinobacteria ) . Thermotoga ( Firmicutes (Bacilli B. licheniformis Bacillus subtilis . ( Synergistetes Thermotoga subterranea Fervidobacterium pennivorans P. miotherma Petrotoga mobilis Methanothermobacter . . . thermautotrophicus

: .

S rRNA 16 :

* 13913988/02/ /02 31/31 : - 13913977/08/ /08 27/27 :

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