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 Xiaoke Hu

1

[email protected]

2

Yantai Institute of Costal Zone Research, Chinese Academy of Sciences, Yantai 264003, PR China Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen 361005, PR China

3

Institute 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 genebased 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 genera at the time of writing, Azomonas, Azomonotrichon, Azorhizophilus, Azotobacter, Chryseomonas, Cellvibrio, Flavimonas, Mesophilobacter, Pseudomonas, Rhizobacter, Rugamonas and Serpens (Parte, 2014; Rediers et al., 2004; Skerman et al., 1980). Although the type genus Pseudomonas, and other two genera, Chryseomonas and Flavimonas, in this family are known as emerging opportunistic pathogens (Carmeli et al., 1999; Holmes et al., 1987; Hugh & Leifson, 1964), the family is well-acknowledged to perform important functions in the rhizosphere by fixing nitrogen in the atmosphere to ammonium which supports and enhances plant growth. (De Smedt et al., 1980; Suarez et al., 2014; Young & Park, 2007). Micro-organisms performing this function are termed as plant growthpromoting rhizobacteria (PGPRs) (Vessey, 2003). Here, a

bacterial strain, affiliated into the family Pseudomonadaceae and showing a distinct function is described. The strain, designated HW001T was isolated from the phycosphere of the potential biofuel-producing microalgae Nannochloropsis oceanica IMET1 in a study investigating the diversity and functions of the bacterial communities associated with this microalga (Wang et al., 2012). Strain HW001T showed a remarkable ability to aggregate N. oceanica IMET1, which could be a novel approach to harvest biofuel-producing microalgae. Results indicated that the strain originated from the Permian groundwater, which was used for cultivating N. oceanica IMET1. Polyphasic taxonomic tests including phylogenetic, genotypic, chemotaxonomic and phenotypic assays were performed to characterize the novel strain in this study and indicated that strain HW001T represents a novel species of a new genus in the family Pseudomonadaceae.

Abbreviations: PE, phosphatidylethanolamine; UAPL, unidentified aminophospholipid.

Permian groundwater used for cultivating the microalga was collected from the Pecos Cenozoic Trough in Imperial, TX, USA (31u 169 16.930 N 102u 409 48.350 W). Photobioreactors (PBR) were constructed to investigate the diversity and functions of bacteria in the phycosphere at different temperatures (15, 25 and 30 uC). The functional bacterium

The GenBank/EMBL/DDBJ accession number for the 16S rRNA gene sequence of strain HW001T is KJ721800. Two supplementary figures and three supplementary tables are available with the online version of this paper.

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HW001T was successfully isolated on Difco marine agar 2216 plates (BD Bioscience) at 30 uC and cryopreserved at 280 uC in marine broth 2216 (BD Bioscience) supplemented with 30 % (v/v) glycerol. After 72 h incubation on marine agar, the aerobic bacterium strain formed circular, flat, yellow colonies. Gram staining was performed according to the method described by Gerhardt et al. (1994). Scanning electron microscopy (SEM) was used to observe the morphology of strain HW001T. The results indicated that strain HW001T was a Gram-stain-negative, rod-shaped (0.461.6–2.7 mm) bacterium (Fig. S1, available in the online Supplementary Material). Genomic DNA was extracted using an Ultra-Clean microbial DNA isolation kit (MoBio Laboratories). PCR amplification and 16S rRNA gene sequencing was performed as described previously (Enticknap et al., 2006). The almost full-length 16S rRNA gene was analysed using the EzTaxon-e server (Kim et al., 2012). 16S rRNA gene sequences were aligned with representative members of selected genera belonging to the family Pseudomonadaceae in the phylum Proteobacteria. Phylogenetic analysis was conducted using the MEGA 4 software package (Tamura et al., 2007). A phylogenetic tree was reconstructed using the neighbour-joining (Jukes–Cantor correction) algorithm. The robustness of the inferred tree topologies was evaluated after 1000 bootstrap replicates of the neighbourjoining data. The taxonomic analysis by using EzTaxon-e shows that strain HW001T is only 88.31 % similar to any previously identified type strain. The closest cultured bacterium was Pseudomonas protegens CHA0T, affiliated into the genus Pseudomonas in the family Pseudomonadaceae. Similarities

65 0.01

of strain HW001T with the type species of each genus in the family Pseudomonadaceae ranged from 82.99 % to 87.45 % (Table S1). Phylogenetic analysis of strain HW001T and all type strains in the family indicated that the novel bacterium does not affiliate into any existing genus and forms a distinct lineage in the family Pseudomonadaceae (Fig. 1, Fig. S2). Temperature, pH, and salinity suitable for the growth of strain HW001T and the reference strain Pseudomonas aeruginosa ATCC 10145T were tested according to previously described methods (Nedashkovskaya et al., 2004a; Yi & Chun, 2004). Physiological and biochemical characterizations were conducted using API ZYM, API 50 CH, API 20NE, API 20E and API 50CHB strips (bioMe´rieux), while some media used for tests were prepared as previously described (Yi et al., 2003). Sensitivity to antibiotics was tested by adding antibiotic discs (Oxoid) onto marine agar plates spread with fresh HW001T cultures. The antibiotics and their minimum inhibitory concentration (MIC; mg ml21) determined in this experiment were as follows: kanamycin (0.5), ceftazidime (0.125), norfloxacin (,0.016), tetracycline (0.38), nitrofurantoin (3), gentamicin (0.125) and chloramphenicol (0.032). The effect of antibiotics on the growth of cells was assessed after 48 h based on the methods described as CLSI/NCCLS M100-S21 (CLSI, 2011). The results of physiological and biochemical tests are given in the species description and in Table 1 and Table S2. Simultaneous tests of all parameters mentioned above were conducted on the reference strain. The DNA G+C content of strain HW001T was determined by using the thermal denaturation method (Mandel & Marmur, 1968). The results showed that the DNA G+C

Azorhizophilus paspali ATCC 23833T (AJ308318) Pseudomonas aeruginosa ATCC 10145T (HE978271)

57 100 66

Azomonotrichon macrocytogenes ATCC 12335T (AB175654) Azotobacter chroococcum ATCC 9043T (AB175653) Serpens flexibilis ATCC 29606T (GU269546) Azomonas agilis ATCC 7494T (AB175652)

99

Chryseomonas polytricha ATCC 43330T (D84003) 53

99

Flavimonas oryzihabitans ATCC 43272T (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 ATCC 43154T (Austin & Moss, 1986), 10, Serpens flexibilis ATCC 29606T (Hespell, 1977). +, Positive; 2, negative; NA, no data available. Characteristic pH range for growth Salinity for growth (%, w/v) Acid production from: (2)-D-Arabinose (2)-L-Xylose (+)-L-Arabinose D-Fructose D-Mannose (+)-Cellobiose (+)-Maltose Starch Gluconate Enzymic activities Urease Catalase Oxidase Hydrolysis of: Maltose Malic acid Sodium citrate Mannitol

1

2

3

4

5

6

7

8

9

10

6–10 2–8

5–10 0–6

5.2–6.9

Neutral and alkaline pH 5–10

NA

NA NA

7.6 7–20

NA

NA

0–0.7

5–9 0–5

5.8–7.2 5.85

2 2 2 2 2 + + + +

+ + + + + 2 2 2 2

2 2 2 2

2 + + + + + + + +

+ + + +

+

+ + + + + + + + +

+ + + + + + + 2 +

2 2 +

+ + 2

+ + +

+ + +

+ + 2

+ 2 2 2

2 + + +

NA

NA NA

2 2 NA

NA

2 + +

2 2 2 +

+ 2 2 2

NA NA

content of the strain HW001T was 55.4 mol%. This value is lower than those associated with members of the genus Pseudomonas, which range from 58–70 mol% (Palleroni, 1984). The Sherlock Microbial Identification System (MIDI) was applied for measuring cellular fatty acids of strain HW001T and the reference strain Pseudomonas aeruginosa ATCC 10145T. Strain HW001T and the reference strain were cultured to late exponential phase in marine broth 2216 at 30 uC for 48 h and Luria broth (LB; Life Technologies) at 37 uC for 48 h, respectively. The predominant cellular fatty acids of strain HW001T were iso-C15 : 0 (29.15 %), isoC15 : 0, summed feature 9 (iso-C17 : 1v9c, 22.25 %), C16 : 0 (7.0 %) and summed feature 3 (C16 : 1v7c/C16 : 1v6c, 6.44 %) (Table S3), while the principal cellular fatty acids for the reference strain were C16 : 0 (31.1 %) and C18 : 1v7c/ C18 : 1v6c (31.86 %). Quinone composition was characterized by HPLC as described previously (Nedashkovskaya et al., 2004b). The main isoprenoid quinone of strain HW001T was Q-8 (ca. 100 %) which was consistent with type species of genera Rhizobacter and Mesophilobacter. Polar lipids were determined using TLC following the method of Minnikin et al. (1984): methanol/water (100 : 10, v/v) and petroleum ether (b.p. 60–80 uC) extraction was applied followed by chloroform/methanol/water (90 : 100 : 30, by vol.) extraction, chloroform/methanol/water (50 : 100 : 40, http://ijs.sgmjournals.org

NA

2 NA

2 2 NA

+ 2

NA

+ + + 2 2 + 2 2 2 + 2

NA NA NA

+ NA

+ + NA

NA NA NA

+ 2 + + NA

+ NA

+ +

+

+

+

+

+

+

NA

NA

NA

NA

NA

NA

+ +

+ +

+

2 +

+

NA

NA

2 2

by vol.) extraction twice, and chloroform/water (1 : 1, v/v) extraction subsequently. Polar lipids were harvested after evaporation of the lower layer with N2 (,37 uC). Chromatography was conducted by using chloroform/ methanol/water (65 : 25 : 4, by vol.), followed by chloroform/acetic acid/methanol/water (40 : 7.5 : 6.2, by vol.). Ethanolic molybdophosphoric acid (5 %) was applied to detect the presence of all lipids. Ninhydrin (0.2 % in watersaturated butanol) was used for revealing the presence of phospholipids. a-Naphthol/sulphuric acid was sprayed to reveal the presence of glycolipids. The results indicated that the polar lipid profile was composed of phosphatidylethanolamine (PE), an unidentified aminophospholipid (UAPL), and some other unidentified lipids (Fig. 2). However, diphosphatidylglycerol, phosphatidylglycerol and phosphatidylcholine, three common polar lipids in the genus Pseudomonas were not detected. The great differences shown by phylogenetic, genotypic, chemotaxonomic and phenotypic analyses distinguished the novel bacterium HW001T from the closest reference strain, Pseudomonas aeruginosa ATCC 10145T. Based on polyphasic analysis in this taxonomic study, strain HW001T represents a novel species of a new genus affiliated with the family Pseudomonadaceae, for which the name Permianibacter aggregans gen. nov., sp. nov. is proposed. 3505

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The type strain is HW001T (5CICC 10856T5KCTC 32485T), isolated from Permian ground water, from the Pecos Cenozoic Trough in Imperial, TX, USA. The DNA G+C content of the type strain is 55.4 mol%. UL UL

UL

PE UAPL

UL

Fig. 2. Polar lipids of strain HW001T separated by twodimensional TLC and detected by spraying with molybdatophosphoric acid reagent. PE, Phosphatidylethanolamine; UAPL, unidentified aminophospholipid; UL, unknown lipid.

Acknowledgements We acknowledge the China Center of Industrial Culture Collection for assistance in identifying the novel strain. Aidan Parte is thanked for nomenclatural advice. Funding for this research was provided by the Hundred Talents Program of Chinese Academy of Sciences awarded to X. H., the Science and Technology Program of Shandong Province (2013GHY11534) and the State Key Laboratory of Marine Environmental Science (Xiamen University) visiting fellowship (MELRS1211). The Permian groundwater was kindly provided by Bart Reid, Organic Aquaculture Institute, Imperial, TX, USA. Funding for H. W. was generously provided by the China Scholarship Council.

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Permianibacter aggregans gen. nov., sp. nov., a bacterium of the family Pseudomonadaceae capable of aggregating potential biofuel-producing microalgae.

A novel bacterial strain, capable of aggregating potential biofuel-producing microalgae, was isolated from the phycosphere of an algal culture and des...
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