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Genes Involved in Alkane Degradation in the Alcanivorax Hongdengensis Strain A-11-3

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Genes Involved in Alkane Degradation in the Alcanivorax Hongdengensis Strain A-11-3 Appl Microbiol Biotechnol (2012) 94:437–448 DOI 10.1007/s00253-011-3818-x APPLIED GENETICS AND MOLECULAR BIOTECHNOLOGY Genes involved in alkane degradation in the Alcanivorax hongdengensis strain A-11-3 Wanpeng Wang & Zongze Shao Received: 13 September 2011 /Revised: 1 December 2011 /Accepted: 5 December 2011 /Published online: 30 December 2011 # Springer-Verlag 2011 Abstract Alcanivorax hongdengensis A-11-3 is a newly degrade short (C8) to long (C36) alkanes that are straight or identified type strain isolated from the surface water of the branched. The ability of A. hongdengensis A-11-3 to thrive Malacca and Singapore Straits that can degrade a wide range in oil-polluted marine environments may be due to this of alkanes. To understand the degradation mechanism of this strain’s multiple systems for alkane degradation and its strain, the genes encoding alkane hydroxylases were range of substrates. obtained by PCR screening and shotgun sequencing of a genomic fosmid library. Six genes involved in alkane deg- Keywords Marine oil pollution . Biodegradation . Alkane radation were found, including alkB1, alkB2, p450-1, p450- hydroxylase . Gene cluster . Alcanivorax hongdengensis 2, p450-3 and almA. Heterogeneous expression analysis confirmed their functions as alkane oxidases in Pseudomo- nas putida GPo12 (pGEc47ΔB) or Pseudomonas fluores- Introduction cens KOB2Δ1. Q-PCR revealed that the transcription of alkB1 and alkB2 was enhanced in the presence of n-alkanes Alkanes are highly reduced compounds of straight, branched C12 to C24; three p450 genes were up-regulated by C8–C16 or cyclic chains of various lengths. In nature, bacterial oxida- n-alkanes at different levels, whereas enhanced expression tion of n-alkanes has been identified worldwide (Head and of almA was observed when strain A-11-3 grew with long- Jones 2006; Smits et al. 2002; van Beilen et al. 2004, 2006; chain alkanes (C24 to C36). In the case of branched alkanes, Wang et al. 2010; Whyte and Smits 2002). Members of the pristane significantly enhanced the expression of alkB1, genus Alcanivorax seem to play a particularly pivotal role in p450-3 and almA. The six genes enable strain A-11-3 to bioremediation of oil spills (Liu and Shao 2005;Schneiker et al. 2006;Wuetal.2009). Alcanivorax spp. are found not only in oil-impacted environments (Head and Jones 2006)but Electronic supplementary material The online version of this article also in the open sea (Wang et al. 2010). The genus Alcani- (doi:10.1007/s00253-011-3818-x) contains supplementary material, vorax currently includes six species including A. borkumensis, which is available to authorized users. A. jadensis, A. venustensis, A. dieselolei, A. hongdengensis : W. Wang Z. Shao (*) and A. balearicus; all of these species were isolated from Key Laboratory of Marine Biogenetic Resources, marine environments except A. balearicus, which was isolated The Third Institute of Oceanography, from a subterranean saline lake (Head and Jones 2006;Liu State Oceanic Administration, Daxue Road 178, and Shao 2005; Schneiker et al. 2006;Wuetal.2009). A. Xiamen 361005, China borkumensis metabolizes a wide range of alkanes, including e-mail: [email protected] linear alkanes (C10–C32), cyclo-alkanes and isoprenoids (Hara W. Wang et al. 2003, 2004). A. dieselolei is a promising candidate for oil e-mail: [email protected] pollution mitigation due to its wide substrate range and hydrocarbon-degrading abilities (Liu and Shao 2005;Liu W. Wang School of Life Sciences, Xiamen University, et al. 2011).ThesuccessofthegenusAlcanivorax may be Xiamen 361005, China due to the ability of the members of this genus to use branched- 438 Appl Microbiol Biotechnol (2012) 94:437–448 chain alkanes more effectively than other hydrocarbon- 2005); cells were then collected from a 10-ml culture and degrading bacteria, giving these species a selective advantage inoculated in 100 ml no carbon source medium ASM (Liu (Hara et al. 2003; Liu et al. 2011). and Shao 2005) in 300-ml Erlenmeyer flasks with 2% (w/v) In prokaryotes, several enzyme systems are involved in crude oil or liquid paraffin (mainly composed of C12–C18 alkane degradation. Integral membrane di-iron alkane hydrox- straight alkanes) as the sole carbon sources and then incu- ylase (AlkB) was the first enzyme discovered to have a role in bated at 28 °C on a rotary shaker (180 rpm for 20 days). alkane oxidation (van Beilen et al. 1994). Subsequently, cyto- Individual flasks were selected at intervals (gently vortex for chrome P450 of the CYP153 family was found to be involved 5 min to mix), and decimal dilutions of the cultures were in the oxidation of C5 to C16 n-alkanes in Acinetobacter made and plated on M2 agar plates for determination of the (Maier and Forster 2001; van Beilen et al. 2006). For long- colony-forming unit (CFU) number. chain alkanes, two oxidases have been identified: the soluble To test the range of n-alkane substrates, ASM medium was flavoprotein alkane monooxygenase LadA in Geobacillus supplemented with 1% (w/v) n-alkanes from C8 to C36 or thermodenitrificans NG80-2 (Feng et al. 2007)andthe pristane as the sole carbon source, respectively. For n-alkanes flavin-binding monooxygenase AlmA in Acinetobacter sp. ranging from C20 to C36, 0.001% (w/v) of plysurf A-210 G DSM 1784 (Throne-Holst et al. 2007). was added into the medium as a dispersant. A set of uninoc- The A. hongdengensis strain A-11-3 was isolated from the ulated bottles was treated in parallel and served as the control. surface water of the Malacca and Singapore Straits (Wu et al. The bottles were incubated at 28 °C on a rotary shaker 2009). Like other hydrocarbonoclastic bacteria, A. hongden- (180 rpm) for 7 days. In each bottle, residual n-alkanes were gensis is present at low or undetectable levels in unpolluted analyzed by gas chromatogram (GC). All experiments were environments but blooms dramatically after an oil spill, be- performed in duplicate. coming the predominant microbe in polluted marine waters (unpublished). Members of this species have been frequently Gas chromatogram (GC) analysis detected in surface water, deep water and sediments of the Pacific Ocean, Atlantic Ocean, Indian Ocean, South China Residual n-alkanes were extracted using a continuous liquid– Sea, Sea of Japan and the Straits of Taiwan by our group and liquid extraction technique. The cultures were transferred to others (unpublished). The wide substrate range and broad the liquid–liquid extractor. The interior of the flask was rinsed geographic distribution of this species indicate its important with hexane, and the washings were poured into the central role in marine oil degradation. This report aimed to identify well of the extractor, which allowed the solvent to rise slowly the key enzymes of A. hongdengensis that are responsible for up through the sample and overflow into the round bottom alkane degradation. reflux flask. The sample was extracted for 24 h, and then, the extract was adjusted to the same volume as that of the original culture, supplemented with 0.005% (w/v) of squalane as an Materials and methods internal standard. Finally, the sample was analyzed by GC for n-alkanes less than C36. The extraction recovery rate was Bacterial strains and growth conditions calculated by comparing the concentration of a specific alkane before and after extraction and was 93.2±3.72% for C8,94.7± T A. hongdengensis A-11-3 (LMG 24624) was originally 3.32% for C12, 95.7±2.27% for C16, 94.7±3.63% for C24, isolated from the surface water of the Malacca and Singa- 92.7±4.27% for C32, 93.5±4.21% for C36 and 92.6±3.07% pore Straits (Wu et al. 2009). Table 1 lists other bacterial for pristane. strainsthatwereusedasrecipient strains and for gene GC analysis was performed using an Agilent Technologies cloning, as well as plasmids used in this study. 6820 N gas chromatograph equipped with an on-column injec- Strain A-11-3 was incubated at 28 °C with shaking at tion, FID detector and SPBTM-5 capillary column (30 m× 200 rpm unless noted otherwise. Escherichia coli and Pseu- 0.53 mm i.d., 1.5 lm thickness). Nitrogen was used as a carrier domonas strains were grown at 30 °C in Luria–Bertani broth and was set at a constant flow rate of 35 ml/min. The oven medium (Luria et al. 1960) and M9 salt medium (Sambrook temperature was set at 150 °C for 5 min and then increased to et al. 1989), respectively. The recombinants of Pseudomonas 280 °C at a rate of 15 °C/min. The injector and detector temper- putida and Pseudomonas fluorescens were grown under con- atures were 280 °C and 350 °C, respectively. ditions previously described by van Beilen et al. (2004). Genomic fosmid library construction and analysis Degradation experiments A genomic library was constructed from strain A-11-3 DNA To test its oil-degrading ability, strain A-11-3 was cultivated using the CopyControlTM HTP fosmid library production kit first in M2 medium as previously described (Liu and Shao with the pCC2FOS vector and the phage T1R-resistant Appl Microbiol Biotechnol (2012) 94:437–448 439 EPI300 E. coli strain (Epicentre, Madison, WI). Briefly, and EMBL databases by blastN (http://www.ncbi.nlm.nih.gov/ high-molecular weight DNA was isolated from cells BLAST/), blastX (http://www.ncbi.nlm.nih.gov/BLAST/)and growninM2usingaWizardgenomicDNApurification Wu-blast (http://www.ebi.ac.uk/blast2/), respectively. The kit (Promega, Madison, WI) and sheared to ~40 kb by results were summarized, and the genomic map of each clone pipetting. The fragments were end repaired, ligated into was predicted. The relevant genes involved in the alkane hy- the fosmid vector and packaged.
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