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Permianibacter Aggregans Gen. Nov., Sp. Nov., a Bacterium of the Family Pseudomonadaceae Capable of Aggregating Potential Biofuel-Producing Microalgae

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Permianibacter Aggregans Gen. Nov., Sp. Nov., a Bacterium of the Family Pseudomonadaceae Capable of Aggregating Potential Biofuel-Producing Microalgae International Journal of Systematic and Evolutionary Microbiology (2014), 64, 3503–3507 DOI 10.1099/ijs.0.065003-0 Permianibacter aggregans gen. nov., sp. nov., a bacterium of the family Pseudomonadaceae capable of aggregating potential biofuel-producing microalgae Hui Wang,1,2,3 Tianling Zheng,2 Russell T. Hill3 and Xiaoke Hu1 Correspondence 1Yantai Institute of Costal Zone Research, Chinese Academy of Sciences, Yantai 264003, Xiaoke Hu PR China [email protected] 2Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, PR China 3Institute of Marine and Environmental Technology, University of Maryland Center for Environmental Science, Baltimore, MD 21202, USA A novel bacterial strain, capable of aggregating potential biofuel-producing microalgae, was isolated from the phycosphere of an algal culture and designated HW001T. The novel bacterial strain was identified on the basis of its phylogenetic, genotypic, chemotaxonomic and phenotypic characteristics in this study. Cells were aerobic, Gram-negative rods. 16S rRNA gene- based phylogenetic analysis revealed that strain HW001T is affiliated with the family Pseudomonadaceae in the phylum Proteobacteria, but forms a distinct clade within this family. The DNA G+C content of strain HW001T was 55.4 mol%. The predominant cellular fatty acids were iso-C15 : 0, summed feature 9 (iso-C17 : 1v9c), C16 : 0 and summed feature 3 (C16 : 1v7c/ C16 : 1v6c). Q-8 was the main respiratory quinone. The polar lipid profile contained phosphatidylethanolamine, an unidentified aminophospholipid and some unidentified lipids. Based on the extensive polyphasic analysis, strain HW001T represents a novel species of a new genus in the family Pseudomonadaceae, for which the name Permianibacter aggregans gen. nov., sp. nov., is proposed. The type strain of the type species is HW001T (5CICC 10856T5KCTC 32485T). The family Pseudomonadaceae comprises 12 different bacterial strain, affiliated into the family Pseudomonadaceae genera at the time of writing, Azomonas, Azomonotrichon, and showing a distinct function is described. The strain, Azorhizophilus, Azotobacter, Chryseomonas, Cellvibrio, designated HW001T was isolated from the phycosphere of Flavimonas, Mesophilobacter, Pseudomonas, Rhizobacter, the potential biofuel-producing microalgae Nannochloropsis Rugamonas and Serpens (Parte, 2014; Rediers et al., 2004; oceanica IMET1 in a study investigating the diversity and Skerman et al., 1980). Although the type genus Pseudo- functions of the bacterial communities associated with this monas, and other two genera, Chryseomonas and Flavi- microalga (Wang et al., 2012). Strain HW001T showed a monas, in this family are known as emerging opportunistic remarkable ability to aggregate N. oceanica IMET1, which pathogens (Carmeli et al., 1999; Holmes et al., 1987; Hugh could be a novel approach to harvest biofuel-producing & Leifson, 1964), the family is well-acknowledged to microalgae. Results indicated that the strain originated perform important functions in the rhizosphere by fixing from the Permian groundwater, which was used for nitrogen in the atmosphere to ammonium which supports cultivating N. oceanica IMET1. Polyphasic taxonomic tests and enhances plant growth. (De Smedt et al., 1980; Suarez including phylogenetic, genotypic, chemotaxonomic and et al., 2014; Young & Park, 2007). Micro-organisms phenotypic assays were performed to characterize the novel T performing this function are termed as plant growth- strain in this study and indicated that strain HW001 promoting rhizobacteria (PGPRs) (Vessey, 2003). Here, a represents a novel species of a new genus in the family Pseudomonadaceae. Abbreviations: PE, phosphatidylethanolamine; UAPL, unidentified ami- Permian groundwater used for cultivating the microalga nophospholipid. was collected from the Pecos Cenozoic Trough in Imperial, The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene TX, USA (31u 169 16.930 N 102u 409 48.350 W). Photobio- sequence of strain HW001T is KJ721800. reactors (PBR) were constructed to investigate the diversity Two supplementary figures and three supplementary tables are available and functions of bacteria in the phycosphere at different with the online version of this paper. temperatures (15, 25 and 30 uC). The functional bacterium 065003 G 2014 IUMS Printed in Great Britain 3503 H. Wang and others HW001T was successfully isolated on Difco marine agar of strain HW001T with the type species of each genus in the 2216 plates (BD Bioscience) at 30 uC and cryopreserved at family Pseudomonadaceae ranged from 82.99 % to 87.45 % 280 uC in marine broth 2216 (BD Bioscience) supple- (Table S1). Phylogenetic analysis of strain HW001T and mented with 30 % (v/v) glycerol. After 72 h incubation all type strains in the family indicated that the novel on marine agar, the aerobic bacterium strain formed bacterium does not affiliate into any existing genus and circular, flat, yellow colonies. Gram staining was performed forms a distinct lineage in the family Pseudomonadaceae according to the method described by Gerhardt et al. (Fig. 1, Fig. S2). (1994). Scanning electron microscopy (SEM) was used to Temperature, pH, and salinity suitable for the growth observe the morphology of strain HW001T. The results of strain HW001T and the reference strain Pseudomonas indicated that strain HW001T was a Gram-stain-negative, aeruginosa ATCC 10145T were tested according to pre- rod-shaped (0.461.6–2.7 mm) bacterium (Fig. S1, avail- viously described methods (Nedashkovskaya et al., 2004a; Yi able in the online Supplementary Material). & Chun, 2004). Physiological and biochemical characteri- Genomic DNA was extracted using an Ultra-Clean zations were conducted using API ZYM, API 50 CH, microbial DNA isolation kit (MoBio Laboratories). PCR API 20NE, API 20E and API 50CHB strips (bioMe´rieux), amplification and 16S rRNA gene sequencing was per- while some media used for tests were prepared as previously formed as described previously (Enticknap et al., 2006). described (Yi et al., 2003). Sensitivity to antibiotics was The almost full-length 16S rRNA gene was analysed using tested by adding antibiotic discs (Oxoid) onto marine agar the EzTaxon-e server (Kim et al., 2012). 16S rRNA gene plates spread with fresh HW001T cultures. The antibiotics sequences were aligned with representative members of and their minimum inhibitory concentration (MIC; mg selected genera belonging to the family Pseudomonadaceae ml21) determined in this experiment were as follows: in the phylum Proteobacteria. Phylogenetic analysis was kanamycin (0.5), ceftazidime (0.125), norfloxacin (,0.016), conducted using the MEGA 4 software package (Tamura tetracycline (0.38), nitrofurantoin (3), gentamicin (0.125) et al., 2007). A phylogenetic tree was reconstructed using and chloramphenicol (0.032). The effect of antibiotics on the neighbour-joining (Jukes–Cantor correction) algo- the growth of cells was assessed after 48 h based on the rithm. The robustness of the inferred tree topologies was methods described as CLSI/NCCLS M100-S21 (CLSI, 2011). evaluated after 1000 bootstrap replicates of the neighbour- The results of physiological and biochemical tests are given joining data. in the species description and in Table 1 and Table S2. Simultaneous tests of all parameters mentioned above were The taxonomic analysis by using EzTaxon-e shows that conducted on the reference strain. strain HW001T is only 88.31 % similar to any previously identified type strain. The closest cultured bacterium was The DNA G+C content of strain HW001T was determined Pseudomonas protegens CHA0T, affiliated into the genus by using the thermal denaturation method (Mandel & Pseudomonas in the family Pseudomonadaceae. Similarities Marmur, 1968). The results showed that the DNA G+C T 65 Azorhizophilus paspali ATCC 23833 (AJ308318) 0.01 Pseudomonas aeruginosa ATCC 10145T (HE978271) 57 Azomonotrichon macrocytogenes ATCC 12335T (AB175654) Azotobacter chroococcum ATCC 9043T (AB175653) 100 66 Serpens flexibilis ATCC 29606T (GU269546) Azomonas agilis ATCC 7494T (AB175652) 99 Chryseomonas polytricha ATCC 43330T (D84003) 53 T 99 Flavimonas oryzihabitans ATCC 43272 (D84004) Cellvibrio mixtus UQM 2601T (AF448515) Permianibacter aggregans HW001T (KJ721800) 100 Rhizobacter dauci ATCC 43778T (AB297965) Rugamonas rubra ATCC 43154T (HM038005) Roseobacter litoralis ATCC 49566T (X78312) Fig. 1. Rooted neighbour-joining tree of partial 16S rRNA gene sequences of strain HW001T and representative members of selected genera belong to the family Pseudomonadaceae in the phylum Proteobacteria. The tree was reconstructed using MEGA software. Roseobacter litoralis ATCC 49566T (GenBank accession no. X78312) was used as the outgroup. Numbers at nodes are bootstrap values (%) based on 1000 replicates. Bar, 0.01 substitutions per nucleotide position. 3504 International Journal of Systematic and Evolutionary Microbiology 64 Permianibacter aggregans gen. nov., sp. nov. Table 1. Differential characteristics of strain HW001T and reference strains in the family Pseudomonadaceae Strains: 1, HW001T,2,Pseudomonas aeruginosa ATCC 10145T (data from this study), 3, Azomonotrichon macrocytogenes ATCC 12335T (De Ley & Park, 1966), 4, Cellvibrio mixtus UQM 2601T (Blackall et al., 1985), 5, Chryseomonas polytricha ATCC 43330T (Holmes et al., 1986), 6, Flavimonas oryzihabitans ATCC 43272T (Holmes et al., 1987), 7, Mesophilobacter marinus IAM 13185T (Nishimura et al., 1989), 8, Rhizobacter dauci ATCC 43778T (Goto & Kuwata, 1988), 9, Rugamonas rubra
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