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Sphingomonas from Petroleum-Contaminated Soils In b r a z i l i a n j o u r n a l o f m i c r o b i o l o g y 4 7 (2 0 1 6) 271–278 ht tp://www.bjmicrobiol.com.br/ Environmental Microbiology Sphingomonas from petroleum-contaminated soils in Shenfu, China and their PAHs degradation abilities a a,b,∗ a a a Lisha Zhou , Hui Li , Ying Zhang , Siqin Han , Hui Xu a Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China b State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, China a r t i c l e i n f o a b s t r a c t Article history: Members of the Sphingomonas genus are often isolated from petroleum-contaminated soils Received 22 October 2012 due to their unique abilities to degrade polycyclic aromatic hydrocarbons (PAHs), which Accepted 17 August 2015 are important for in situ bioremediation. In this study, a combined phenotypic and geno- Available online 2 March 2016 typic approach using streptomycin-containing medium and Sphingomonas-specific PCR was developed to isolate and identify culturable Sphingomonas strains present in petroleum- Associate Editor: Rodrigo Costa contaminated soils in the Shenfu wastewater irrigation zone. Of the 15 soil samples examined, 12 soils yielded yellow streptomycin-resistant colonies. The largest number of Keywords: 5 −1 yellow colony-forming units (CFUs) could reach 10 CFUs g soil. The number of yellow CFUs Sphingomonas had a significant positive correlation (p < 0.05) with the ratio of PAHs to total petroleum Polycyclic aromatic hydrocarbons hydrocarbons (TPH), indicating that Sphingomonas may play a key role in degrading the PAH (PAHs) fraction of the petroleum contaminants at this site. Sixty yellow colonies were selected ran- Degradation domly and analyzed by colony PCR using Sphingomonas-specific primers, out of which 48 Genus isolates had PCR-positive signals. The 48 positive amplicons generated 8 distinct restriction fragment length polymorphism (RFLP) patterns, and 7 out of 8 phylotypes were identified as Sphingomonas by 16S rRNA gene sequencing of the representative strains. Within these 7 Sphingomonas strains, 6 strains were capable of using fluorene as the sole carbon source, while 2 strains were phenanthrene-degrading Sphingomonas. To the best of our knowledge, this is the first report to evaluate the relationship between PAHs contamination levels and culturable Sphingomonas in environmental samples. © 2016 Sociedade Brasileira de Microbiologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). ∗ Corresponding author. E-mail: [email protected] (H. Li). http://dx.doi.org/10.1016/j.bjm.2016.01.001 1517-8382/© 2016 Sociedade Brasileira de Microbiologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 272 b r a z i l i a n j o u r n a l o f m i c r o b i o l o g y 4 7 (2 0 1 6) 271–278 the contamination level by the direct and specific detection Introduction of culturable Sphingomonas from the soils. Additionally, the PAH-degrading capability of the isolated Sphingomonas was Polycyclic aromatic hydrocarbons (PAHs) are considered haz- preliminarily characterized. ardous due to their toxic, genotoxic, mutagenic and/or 1 carcinogenic properties. Microbial degradation is a major process in the successful removal and elimination of PAHs Materials and methods 2 from contaminated soils. The use of native or indige- nous microbiota is of great interest for bioremediation of Soil samples petroleum-polluted sites because they are often more useful and beneficial than commercial inocula that can be out- Soil samples were collected from the Shenfu 3 ◦ ◦ competed by indigenous microorganisms. wastewater irrigation zone (41 50 46 –41 41 24 N, ◦ ◦ Members of the genus Sphingomonas, which was pro- 123 44 43 –123 25 38 E), which is the biggest petroleum 4 posed by Yabuuchi et al., are frequently isolated from wastewater irrigation zone in China. The total length of the PAH-contaminated soils, suggesting that the Sphingomonas are irrigation channel is approximately 70 km, and 15 sampling probably key members of natural PAH-degrading microbial sites with different relative geographical positions, irrigation 3,5,6 consortia. A number of studies demonstrated that Sphin- histories and soil management types were selected from up- gomonas was one of the dominant populations in the microbial to down-stream. The 15 sampling sites included 11 paddy 7–9 communities of PAH-contaminated soil and water samples. soils (soils A–K) and 4 upland soils (soils L, M, N and O) that The Shenfu irrigation zone is located between Shenyang were referred to as soils A–O in the following text. The phys- and Fushun city in Liaoning province and is the largest icochemical soil characteristics and the PAH concentrations 11 petroleum wastewater irrigation zone in China. The paddy in the soil were reported in our previous study. Typically, fields in this region have been irrigated by oil-bearing waste- soil samples collected from the up- and mid-stream sites water discharged by the petroleum and coal-refining industry accumulated more petroleum contaminants compared with since the 1940s due to a lack of irrigation water. During the those from the down-stream sites. 1980–1990s, partial paddy fields were converted to upland in the up- and mid-stream. Mineral oil (especially PAHs) was the Selective isolation and enumeration of putative 10 dominant contaminant in the Shenfu irrigation zone. Our Sphingomonas previous study demonstrated that a large percentage of Sphin- gomonas species was present in the petroleum-contaminated The indigenous putative culturable Sphingomonas were iso- 12 soils of the Shenfu irrigation area using culture-independent lated and enumerated using a previously described method. 11 methods, indicating a potential link between Sphingomonas The streptomycin-resistant yellow colonies that occurred on and the biodegradation of petroleum compounds in the the plates were counted based on the formation of colony Shenfu irrigation zone. However, due to the lack of a reliable forming units (CFUs). system for the specific detection and isolation of culturable Sphingomonas, the functional strains in the environmental PCR and RFLP analysis of the Sphingomonas isolates samples were only found at random. 12 Vanbroekhoven et al. developed a streptomycin-based The identity of the yellow colonies grown on the streptomycin Sphingomonas growth medium that, together with the yel- plates was confirmed by genus-specific colony PCR. The PCR low pigmentation of Sphingomonas, facilitated the detection protocol was used with the SA429f/933r primer set developed 17 and isolation of culturable Sphingomonas from soils. However, in our previous study. The amplicons with the expected size this phenotypic detection method is not efficient or accurate were further analyzed by RFLP analysis using three endonucle- ◦ because other bacterial taxa also produce yellow pigments ases [HaeIII (GG CC), HinfI (G ANTC) and MspI (C CGG)] at 37 C and are resistant to streptomycin. A genotypic detection for 2 h. The RFLP patterns were compared manually, and dis- method that circumvents the major drawbacks inherent in the tinguishable RFLP patterns were considered to represent one phenotypic detection method described above has been devel- phylotype. oped for the detection of specific groups. The 16S rRNA gene sequence offers ample possibilities to distinguish microorgan- Phylogenetic identification of Sphingomonas isolates isms of various genera and minimize false-positive reactions 13,14 using genus-specific primers. PCR-based detection has Tw o representatives of each phylotype were selected for proven to be useful for the identification of the genera nearly full-length 16S rRNA gene sequencing for phylogenetic Clostridium, Pseudonocardia, Saccharopolyspora, Nocardiopsis and identification. PCR amplification of the 16S rRNA genes was 14–16 Saccharothrix using genus-specific primers. In our previous performed with the forward primer 27F and the reverse primer 18 study, a primer set targeting the Sphingomonas 16S rRNA gene 1492R. The obtained sequences were used for phylogenetic 17 11 was designed ; thus, we hypothesized that the use of genus- analysis as described previously. specific colony PCR combined with phenotypic identification would allow the specific detection of Sphingomonas isolates. Measurement of PAH degradation The specific aim of this study was to investigate the rela- tionship between indigenous culturable Sphingomonas in soils To determine the PAH-degrading capability of the iso- from the Shenfu petroleum-wastewater irrigation zone and lated Sphingomonas strains, the pure strains were inoculated b r a z i l i a n j o u r n a l o f m i c r o b i o l o g y 4 7 (2 0 1 6) 271–278 273 into mineral salts medium (MSM) containing a single PAH Previous real-time PCR analysis indicated that all 15 compound as the sole carbon and energy source. The MSM petroleum-contaminated soil samples gave positive signals 11 at pH 7.0–7.2 contained 2 g K2HPO4, 0.5 g KH2PO4, 0.5 g for Sphingomonas. However, in this study only 12 soils NaCl, 0.5 g NH4Cl, 0.2 g MgSO4, 10 mg CaCl2, and 1 ml of yielded yellow colonies on the selective LB plates with 3 × trace element solution per liter of water. The composi- Sm. The number of yellow CFUs ranged from 0.6 10 to −1 5 −1 × tion of the trace element solution was 2 g L FeSO4·7H2O, 1.6 10 CFUs g soil (Table 1). Provided that all of the yellow −1 −1 −1 2 g L MnSO4·H2O, 0.5 g L Na2MoSO4·2H2O, 0.2 g L H3BO4, colonies belonged to the Sphingomonas genus, the counts of the −1 −1 −1 5 −1 0.4 g L CuSO4·5H2O, 0.5 g L ZnSO4, 0.2 g L NH4VO3, Sphingomonas strains could only reach 10 CFUs g soil, which −1 −1 7 8 −1 0.5 g L CoCl2·6H2O, and 0.2 g L NiCl2·6H2O.
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