Open Access

Antibacterial activity of aquatic gliding bacteria

  • Yutthapong Sangnoi1Email author,
  • Theerasak Anantapong2 and
  • Akkharawit Kanjana-Opas2
SpringerPlus20165:116

https://doi.org/10.1186/s40064-016-1747-y

Received: 16 February 2015

Accepted: 28 January 2016

Published: 4 February 2016

Abstract

The study aimed to screen and isolate strains of freshwater aquatic gliding bacteria, and to investigate their antibacterial activity against seven common pathogenic bacteria. Submerged specimens were collected and isolated for aquatic gliding bacteria using four different isolation media (DW, MA, SAP2, and Vy/2). Gliding bacteria identification was performed by 16S rRNA gene sequencing and phylogenetic analysis. Crude extracts were obtained by methanol extraction. Antibacterial activity against seven pathogenic bacteria was examined by agar-well diffusion assay. Five strains of aquatic gliding bacteria including RPD001, RPD008, RPD018, RPD027 and RPD049 were isolated. Each submerged biofilm and plastic specimen provided two isolates of gliding bacteria, whereas plant debris gave only one isolate. Two strains of gliding bacteria were obtained from each DW and Vy/2 isolation medium, while one strain was obtained from the SAP2 medium. Gliding bacteria strains RPD001, RPD008 and RPD018 were identified as Flavobacterium anhuiense with 96, 82 and 96 % similarity, respectively. Strains RPD049 and RPD027 were identified as F. johnsoniae and Lysobacter brunescens, respectively, with similarity equal to 96 %. Only crude extract obtained from RPD001 inhibited growth of Listeria monocytogenes (MIC 150 µg/ml), Staphylococcus aureus (MIC 75 µg/ml) and Vibrio cholerae (MIC 300 µg/ml), but showed weak inhibitory effect on Salmonella typhimurium (MIC > 300 µg/ml). Gliding bacterium strain RPD008 should be considered to a novel genus separate from Flavobacterium due to its low similarity value. Crude extract produced by RPD001 showed potential for development as a broad antibiotic agent.

Keywords

Aquatic gliding bacteria Antibacterial activity Pathogenic bacteria Isolation media Agar-well diffusion assay Biofilm Novel genus

Background

Gliding bacteria are characterized as Gram negative, unicellular, swarm-colony-producing and uniquely motile by the ability to glide on surfaces. They are commonly found in various terrestrial, fresh, and seawater environments (Dawid 2000). These microorganisms play an important role in the degradation of plants and animal debris in many environments. The genera Flavobacterium and Lysobacter are gliding bacteria belonging to phyla Bacteroidetes and Proteobacteria, respectively. These genera are typically founded in plant, soil, and aquatic habitats. In recent years, isolation reports for Flavobacterium including F. anhuiense, F. tiangeerense, F. ginsengiterrae, F. compostarboris, F. hauense, F. aquaticum, F. limnosediminis, F. longum and F. urocaniciphilum, F. panaciterrae, F. lacus, and F. faecale have been released (Dong et al. 2013; Fujii et al. 2014; Jin et al. 2014; Kim et al. 2011, 2012, 2014; Lee et al. 2013; Li et al. 2014; Liu et al. 2008; Subhash et al. 2013; Xin et al. 2009). In addition, papers describing the isolation of new Lysobacter strains including L. capsici, L. ximonensis, L. oryzae, L. soli, L. korlensis and L. bugurensis, L. arseniciresistens, L. oligotrophicus, and L. panacisoli have been published (Aslam et al. 2009; Choi et al. 2014; Fukuda et al. 2013; Luo et al. 2012; Park et al. 2008; Srinivasan et al. 2010; Wang et al. 2009; Zhang et al. 2011). Despite the need for intensive isolation procedures, the screening of these two genera for antimicrobial properties was conducted for the purpose of potential antibiological applications. Genus Flavobacterium inhabits both terrestrial and aquatic environments. Several strains, such as F. psychrophilum, F. columnare and F. spartansii are known as fish pathogens (Cerro et al. 2010; Loch and Faisal 2014; Verma and Rathore 2013). However, few research studies investigating their biological activities have been published. The isolation of the β-lactam antibiotic deacetoxycephalosporin C, from Flavobacterium sp. SC 12,154 was reported by Singh et al. (1982). Another substance, monoacyldiglycosyl-monoacylglycerol was obtained from F. marinotypicum (Yagi and Maruyama 1999). The antimicrobial metabolites extracted from genus Lysobacter have been reported several times. Lysobactin, a potent antibiotic compound, was first isolated from Lysobacter sp. in 1988 by Bonner et al. (1988) and O’Sullivan et al. (1988). Tripopeptins were obtained from another strain of this microorganism in 2001 (Hashizume et al. 2001). Subsequently, strong antimicrobial metabolites isolated from the newly-discovered species L. capsici demonstrated abilities to inhibit the growth of bacteria, yeast, and fungi (Park et al. 2008). Moreover, L. enzymogenes C3 and Lysobacter sp. SB-K88 exhibited antagonistic activity against multiple plant pathogens (Islam 2010; Li et al. 2008). This indicated that Lysobacter spp. were bio-control bacteria capable of inhibiting plant diseases. Thus, the present study aimed to isolate and examine the antibacterial activity of aquatic gliding bacteria.

Methods

Isolation and purification

The submerged or moistened specimens including plant debris, algae, sediments, plastics, metal pieces, biofilms, and animal dungs were collected from the plant genetic resources conservation area at Cheow Lan Reservoir in Surat Thani province, Southern Thailand (GPS location: 8.5814 N 98.4830 E). Fifty-four specimens were subjected to a gliding bacterial isolation program using four different isolation media: DW (agar 15 g; distilled water 1 l), modified MA (peptone 5 g, yeast extracts 1 g, MgCl 9 g, NaSO4 4 g, CaCl 2 g, agar 15 g, distilled water 1 l), SAP2 (tryptone 1 g, yeast extracts 1 g, agar 15 g, distilled water 1 l), and Vy/2 (baker’s yeast paste 5 g, agar 15 g, distilled water 1 l) (Sangnoi et al. 2009). Specimens were carefully cut into small pieces, then placed directly onto each type of isolation medium and incubated at room temperature. After the microorganisms displayed motility by gliding, the spread of the swarm colony was observed. After that, a clean edge of each swarm colony was sliced off and sub-cultured using another fresh isolation medium. Pure cultures were obtained by repeat sub-culturing 5–6 times. The pure strains were maintained on SAP2 agar medium at 4 °C for working strains, and fresh cells were preserved in 20 % glycerol at −20 °C for long term preservation.

Morphological, physiological, and biochemical analysis

Cell morphology and gliding motility were observed using an Olympus BX50 light microscope with a drop of lactophenol blue added to enhance observational ability. A slide with thin SAP2 agar medium overlay was used to examine gliding motility. After placing a swarm colony on an overlay and allowing incubation, we observed gliding motility. Catalase activity was tested by bubble formation in 3 % H2O2 solution. Oxidase activity was determined by the oxidation of 1 % tetramethyl-p-phenylenediamine on filter paper. Acid production from carbohydrates was investigated using the commercial API 50 CH and API 20 E systems (BIOMERIEUX). Enzyme production was tested using the commercial API ZYM system (BIOMERIEUX), in accordance with manufacturer instructions.

16S rRNA gene sequence and phylogenetic analysis

The genomic DNA of the isolates was extracted using a Genomic DNA mini-kit (Geneaid) to determine phylogenetic relationships. The 16S rRNA genes were amplified by PCR using a set of 16S rRNA gene universal primers 27F (5′-AGAGTTTGATCATGGCTCAG-3′) and 1492R (5′-GGTACCTTGTTACGACTT-3′). The amplified PCR products were purified by GF-1 AmbiClean Kit (PCR/Gel) (Vivantis). Sequencing reactions were performed with the same universal primers, manufactured by First BASE Laboratories Sdn Bhd’s. Partial DNA sequences were compared with related sequences using the BLAST program, part of the GenBank/EMBL/DDBJ database (Altschul et al. 1990). Multiple alignments of the 16S rRNA gene sequences were carried out using the CLUSTAL_X program, version 1.83 (Thomson et al. 1997). Nucleotide substitution rates (K nuc values) were determined (Kimura 1983), and the phylogenetic tree was constructed using the MEGA 5.22 program (Tamura et al. 2011). A bootstrap value test was performed with 1000 replicates, and a phylogenetic tree was determined using neighbor-joining, maximum-parsimony, and maximum-likelihood methods (Felsenstein 1985; Saitou and Nei 1987).

Crude extract preparation

Each gliding bacterial isolate was cultivated in a 250 ml Erlenmeyer flask containing 100 ml of SAP2 broth medium and 2 g of amberlite XAD-16 resins (Sangnoi et al. 2008, 2009, 2014; Spyere et al. 2003). The cultivation flasks were incubated and shaken at 200 rpm for 7 days at 25 °C. The resins were collected using a nylon mesh and rinsed with deionized water to remove unwanted cells and other contaminants. Resins were left to dry at room temperature for 15 min and also soaked in 100 ml methanol for 1 h. Methanolic phases were separated from the resins, and methanolic crude extracts were obtained after evaporating a methanol solvent (Sangnoi et al. 2008, 2009, 2014). Crude extracts were prepared to a final concentration of 25 mg/ml in DMSO.

Antibacterial assay

The agar-well diffusion assay as described by Wonghirundecha et al. (2014) was performed in this study to determine the antibacterial activity of gliding bacterial crude extract. Crude extracts were tested for antibacterial activity against seven pathogenic bacteria: Vibrio cholerae non O1/non O139 DMST 2873, Listeria monocytogenes DMST 1327, Escherichia coli DMST 4212, Bacillus cereus DMST 5040, Salmonella typhimurium DMST 562, Staphylococcus aureus DMST 8840 and Serratia marcescens TISTR 1354. Tested strains were activated twice in NB broth (at 37 °C, 18 h) and prepared to a turbidity of 0.5 McFarland standards (approximately 105–106 CFU/ml) as an inoculum. One milliliter of an inoculum was well poured into 9 ml of Muller-Hinton soft medium (0.75 % agar, w/v) in a Petri dish. While those dishes were being solidified, six wells (6 mm in diameter) were drilled into each plate. Methanolic crude extracts were prepared to a final concentration of 25 mg/ml, and aliquots (100 µl) were tested by filling each well. DMSO and tetracycline were used as the negative and positive controls, respectively. Tested plates were incubated at 37 °C for 24 h and then monitored for inhibitory clear zones around the wells. The test for each crude extract against each pathogenic strain was carried out three times. The antibacterial activity was determined as the minimal inhibitory concentration (MIC) value, which is the minimum concentration of the extract that could inhibit the growth of tested microorganisms.

Nucleotide sequence accession numbers

The GenBank/EMBL/DDBJ accession numbers for the partial 16S rRNA gene sequences of the strains were RPD001, RPD008, RPD018, RPD027, and RPD049 are AB872448, AB872449, AB872450, AB872451, and AB872452, respectively.

Results

Isolation of aquatic gliding bacteria

Five isolates of aquatic gliding bacteria including strains RPD001, RPD008, RPD018, RPD027, and RPD049 were isolated from 54 specimens collected from Cheow Lan Reservoir. Although many types of specimens were used in the attempt to isolate gliding bacteria, only biofilms, plastics, and plant debris were found to provide the bacteria. Biofilms and plastics were the prolific sources of the aquatic gliding bacteria for this study. Two strains including RPD001 and RPD027 were isolated from biofilms. Also, RPD008 and RPD018 were obtained from plastics. In addition, one isolate (RPD049) was from plant debris. During the isolation program with four different isolation media, two strains of aquatic gliding bacteria (RPD027 and RPD049) were isolated using a DW medium, and two strains (RPD001 and RPD018) were obtained from a Vy/2 medium. One strain (RPD008) was achieved from a SAP2 medium (Table 1). However, no strains were isolated by modified MA medium.
Table 1

The isolation result of aquatic gliding bacteria

Strain

RPD001

RPD008

RPD018

RPD027

RPD049

Type of specimen

Biofilms

Plastic

Plastic

Biofilms

Plant debris

Isolation medium

Vy/2

SAP2

Vy/2

DW

DW

RPD is Cheow Lan Reservoir, where specimens were collected. Vy/2 is medium contained baker’s yeast paste. SAP2 is medium contained tryptone and yeast extracts. DW is a medium containing only distilled water

Morphological, physiological and biochemical characteristics

All five strains were Gram negative, aerobic, non-fruiting body, non-flagellate gliding bacteria. Strain RPD001 was filament shaped and 5–10 µm in length, while other four strains were shaped as short rods, ranging from 0.2 to 0.6 µm in length (Fig. 1). Swarm colony colors of strains RPD001, RPD008, and RPD018 were yellow, whereas strains RPD027 and RPD049 were pale-bright. The phenotypic, morphological, physiological and biochemical features of the isolates are summarized in Table 2. Some characterization of RPD008 was described here because its 16S rRNA sequence data showed a low similarity value to neighbor species (see below), indicating that it might be possible to propose as a novel genus. The main characteristics of RPD008 were described: its growth occurred under a 20–40 °C temperature range, with optimal growth observed at 30–35 °C. Tryptone and yeast extract were useful nitrogen sources for growth. Enzyme activities were positive for esterase (C4), esterase lipase (C8), and naphthol-AS-BI-phosphohydrolase. Acid production was produced from glycerol, D-arabinose, ribose, glucose, fructose, cellobiose, maltose, sucrose, starch, raffinose and L-fucose. Hydrolysis production was only positive for urea. RPD008 was isolated from plastics collected from Cheow Lan Reservoir, Surat Thani province, Southern Thailand.
Fig. 1

Cell morphology of aquatic gliding bacterial strains 1 RPD001 (bar 5 µm), 2 RPD008, 3 RPD018, 4 RPD027, and 5 RPD049 (2–5, bars 1 µm)

Table 2

Phenotypic characteristics of the aquatic gliding bacterial isolates

Characteristic

RPD001

RPD008

RPD018

RPD027

RPD049

Cell morphology

Filament

Rod

Rod

Rod

Rod

Size in length (µm)

5–10

0.2–0.5

0.2–0.4

0.2–0.4

0.2–0.6

Colony color

Yellow

Yellow

Yellow

Pale-bright

Pale-bright

Gliding motility

+

+

+

+

+

Gram’s stain

Negative

Negative

Negative

Negative

Negative

Oxidase

Catalase

+

Enzyme activities

 Alkaline phosphatase

+

+

+

 Esterase (C4)

+

+

+

+

+

 Esterase lipase (C8)

+

+

+

+

+

 Lipase (C14)

+

 Acid phophatase

+

+

 Naphthol-AS-BI-phosphohydrolase

+

+

+

+

+

 β-Galactosidase

+

Hydrolysis of

 Arginine

+

+

 Sodium citrate

+

+

 Urea

+

+

+

+

 Tryptophan

+

 Sodium pyruvate

+

+

 Kohn’s gelatin

+

Acid production of

 d-Arabinose

+

+

 l-Arabinose

+

 Ribose

+

+

+

+

 d-Xylose

+

+

 Galactose

+

 Glucose

+

+

+

 Fructose

+

+

+

+

 Mannose

+

+

 Mannitol

+

 Esculin

+

+

 Cellobiose

+

+

+

+

 Maltose

+

+

+

+

 Sucrose

+

+

+

+

 Starch

+

+

+

+

 Raffinose

+

+

+

 d-Fucose

+

+

+

 l-Fucose

+

+

 5-Keto-gluconate

+

+

 Glycerol

+

+

+

+

RPD is Cheow Lan Reservoir, where specimens were collected

16S rRNA gene sequence and phylogenetic analyses

Phylogenetic analysis of the partial 16S rRNA gene sequence data of the aquatic gliding bacterial strains placed them all into one of two distinct phyla: Bacteroidetes, which belongs to family Flavobacteriaceae within the genus Flavobacterium; and Proteobacteria, which belongs to the family Xanthomonadaceae, within the genus Lysobacter. A blast search with the 16S rRNA gene sequences of strain RPD008 had similarity of 82 % to Flavobacterium anhuiense F11T (JQ579648). Other strains RPD001 and RPD018, and RPD049 had similarity of 96 % to F. anhuiense F11T (JQ579648) and F. johnsoniae 188T (EU730945), respectively. Another strain RPD027 had similarity of 96 % to Lysobacter brunescens KCTC 12130T (AB161360) (Fig. 2). On the basis of the16S rRNA gene sequencing, the strain RPD008 showed a noteworthy sequencing similarity value of less than 90 % and the phylogenetic tree formed a distinct lineage separating from F. anhuiense F11T (Fig. 2).
Fig. 2

Phylogenetic tree of partial 16S rRNA gene sequences of aquatic gliding bacteria isolated from Cheow Lan Reservoir and their neighbor species (bar 0.05)

Antibacterial activity

Methanolic crude extracts of all five gliding bacterial strains were examined for antibacterial activity against pathogenic bacteria including three Gram positive bacteria (B. cereus, L. monocytogenes, and S. aureus) and four Gram negative bacteria (E. coli, S. typhimurium, S. marcescens, and V. cholerae). Antibacterial assay showed that crude extracts produced from four gliding bacteria strains (RPD008, RPD018, RPD027, and RPD049) exhibited no inhibitory clear zone against all tested pathogenic strains. It was noted that only another crude extract obtained from strain RPD001 (96 % similarity with Flavobacterium anhuiense) exhibited an inhibitory clear zone (Fig. 3). The obtained extract showed strong inhibitory activity against both Gram positive and Gram negative pathogenic bacteria including L. monocytogenes (MIC 150 µg/ml), S. aureus (MIC 75 µg/ml), and V. cholerae (MIC 300 µg/ml) (Table 3). However the extract exhibited a weak inhibitory effect on Salmonella typhimurium (MIC > 300 µg/ml) (Fig. 3).
Fig. 3

Inhibitory clear zone on agar-well diffusion plates of crude extract obtained from strain RPD001 (top well of each plate) against 1 Vibrio cholerae non O1/non O139 DMST 2873, 2 Listeria monocytogenes DMST 1327, 3 Staphylococcus aureus DMST 8840, and 4 Salmonella typhimurium DMST 562. Tetracycline (central well of each plate) was used as a positive control

Table 3

Antibacterial spectra of crude extract produced from RPD001 against pathogenic strains

Test pathogenic bacteria

MIC (µg/ml)

Gram positive

 Bacillus cereus DMST 5040

>300

 Listeria monocytogenes DMST 1327

150

 Staphylococcus aureus DMST 8840

75

Gram negative

 Escherichia coli DMST 4212

>300

 Salmonella typhimurium DMST 562

>300

 Serratia marcescens TISTR 1354

>300

 Vibrio cholerae non O1/non O139 DMST 2873

300

MIC is the minimal inhibitory concentration

Discussion

In this study, biofilms and plastics yielded the highest numbers of aquatic gliding bacteria. Biofilms are consortium layers of microorganisms occurring on the surfaces of most submerged substrates (Kadouri and O’Toole 2005). Hence, specimens collected from a submerged plastic surface covered with biofilms should be defined as ‘biofilms on plastic’. Many reports have indicated that biofilms are good sources for isolation of gliding bacteria (Donachie et al. 2004; Kwon et al. 2006; Rickard et al. 2005; Sangnoi et al. 2009; Vandecandelaere et al. 2009). The reasons for this may be because gliding bacteria play an important role in the biodegradation of organic compounds such as exopolysaccharides, which is commonly found in biofilms (Barbeyron et al. 2001; Johansen et al. 1999), and/or because gliding bacteria are ‘pioneer’ species that attach to substrates before development into fully-functioning biofilms. The isolation results of the gliding bacteria under study may depended on the composition of the isolation media, which is the nutrient source for gliding bacteria. DW medium is a growth-limiting nutrient containing only agar and distilled water. This medium might help to eliminate fast-growing species while enriching the relatively slow-growing gliding bacteria. However, it was time-consuming to obtain pure culture from this media, which is also subject to the risk of attack by fungi. In a previous study, our group used another growth-limiting nutrient medium known as SWG medium, which contains only sodium glutamate, sodium chloride, agar and distilled water, to isolate marine gliding bacteria. We found that a SWG medium was effective for marine gliding bacteria isolation (Hosoya et al. 2006, 2007, Sangnoi et al. 2008, 2009; Srisukchayakul et al. 2007). In this study we tried to design a new simple medium (DW) for isolation of fresh water gliding bacteria. We expected that a growth-limiting nutrient medium like DW would be suitable for isolation of slow-growing gliding bacteria that inhabit fresh water environments. In contrast, the Vy/2 medium contained a baker’s yeast paste (yeast cells), which released organic nutrients like amino acids, proteins, carbohydrates, fatty acids, vitamins, minerals, and other growth factors after autoclaving. This enrichment medium was suggested for fast-growing gliding bacteria isolation. However, these organic components are not only required by fast-growing gliding bacteria, but also by other bacterial contaminants. Thus, this medium enables both gliding bacteria and unwanted bacteria to flourish. As a result, an increased frequency of repeated subculturing is required to isolate the gliding bacteria strains under study from the contaminants. The 16S rRNA gene sequence analysis of RPD008 showed less than 90 % similarity value and the phylogenetic tree exhibited clearly separated lineage from related species. These results indicate that the strain RPD008 should be characterized as a novel genus, differentiated from Flavobacterium. However, determination of more chemotaxonomic characteristics such as cellular fatty acid profile, respiratory quinone and G+C content should be the subject of further study. Likewise, three strains (RPD001, RPD018 and RPD049) of genus Flavobacterium and one strain (RPD027) of genus Lysobacter may have the opportunity to be proposed as new species with 96 % similarity value. However, DNA–DNA hybridization experiments with closely-related species of candidate strains must be performed to confirm this presumption. As for antibacterial activity, only crude extract obtained from strain RPD001 was found to show inhibitory effects against pathogenic bacteria. Bioactive compounds composed in this crude extract may have had broad activity because they inhibited both Gram positive and Gram negative pathogenic bacteria. The result suggested the possibility that crude extract produced from strain RPD001 could be developed for use as a broad antibiotic agent. However, the structure elucidation of bioactive compounds and other biological assay of this strain also require further study. In this study, crude extracts obtained from other strains showed no significant antibacterial activity. However, several antibiotics isolated from Flavobacterium and Lysobacter have been reported by other researchers (Bonner et al. 1988; Hashizume et al. 2001; Islam 2010; Li et al. 2008; O’Sullivan et al. 1988; Park et al. 2008; Singh et al. 1982; Yagi and Maruyama 1999). We suggest that these crude extracts may exhibit other biological activities if more biological assays are conducted.

Conclusion

The study results indicated that biofilms on substrates were the good source for aquatic gliding bacteria isolation. Growth-limiting nutrient medium (DW) was suitable for slow-growing gliding bacteria, while a more nutrient-rich medium (Vy/2) was suitable for fast-growing gliding bacteria. Strain RPD008 should be classified as a novel genus due to its low similarity value. Crude extract produced from strain RPD001 showed inhibitory effects against Gram positive and Gram negative pathogenic bacteria; it could possibly be developed as a broad antibiotic agent.

Declarations

Authors’ contributions

YS and AKO designed the research. YS collected specimens, isolated and purified gliding bacteria. YS and TA identified and classified gliding bacteria and examined their antibacterial activity. YS drafted the manuscript, which was proofread by AKO. All authors read and approved the final manuscript.

Acknowledgements

This research work was supported by the Thailand Research Fund (MRG5480237). The authors wish to thank Asst. Prof. Punnanee Sumpavapol of the Faculty of Agro-Industry, Prince of Songkla University, for her kind contribution in preparing antibacterial assay.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors’ Affiliations

(1)
Department of Aquatic Science, Faculty of Natural Resources, Prince of Songkla University
(2)
Department of Industrial Biotechnology, Faculty of Agro-Industry, Prince of Songkla University

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410View ArticleGoogle Scholar
  2. Aslam Z, Yasir M, Jeon CK, Chung YR (2009) Lysobacter oryzae sp. nov., isolated from the rhizosphere of rice (Oryza sativa L.). Int J Syst Evol Microbiol 59:675–680View ArticleGoogle Scholar
  3. Barbeyron T, L’Harido H, Corre E, Kloareg B, Potin P (2001) Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of [Cytophaga] uliginosa (ZoBell and Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. Int J Syst Evol Microbiol 51:985–997View ArticleGoogle Scholar
  4. Bonner DP, O’Sullivan J, Tanaka SK, Clark JM, Whitney RR (1988) Lysobactin, a novel antibacterial agent produced by Lysobacter sp. II. Biological properties. J Antibiot 51:1745–1751View ArticleGoogle Scholar
  5. Cerro AD, Marquez I, Prieto JM (2010) Genetic diversity and antimicrobial resistance of Flavobacterium psychrophilum isolated from cultured rainbow trout, Onchorynchus mykiss (Walbaum), in Spain. J Fish Dis 33:285–291View ArticleGoogle Scholar
  6. Choi JH, Seok JH, Cha JH, Cha CJ (2014) Lysobacter panacisoli sp. nov., isolated from ginseng soil. Int J Syst Evol Microbiol 64:2193–2197View ArticleGoogle Scholar
  7. Dawid W (2000) Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev 24:403–427View ArticleGoogle Scholar
  8. Donachie SP, Bowman JP, Alam M (2004) Psychroflexus tropicus sp. nov., an obligately halophilic CytophagaFlavobacteriumBacteroides group bacterium from an Hawaiian hypersaline lake. Int J Syst Evol Microbiol 54:935–940View ArticleGoogle Scholar
  9. Dong K, Xu B, Zhu F, Wang G (2013) Flavobacterium hauense sp. nov., isolated from soil and emended descriptions of Flavobacterium subsaxonicum, Flavobacterium beibuense and Flavobacterium rivuli. Int J Syst Evol Microbiol 63:3237–3242View ArticleGoogle Scholar
  10. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791View ArticleGoogle Scholar
  11. Fujii D, Nagai F, Watanabe Y, Shirasawa Y (2014) Flavobacterium longum sp. nov. and Flavobacterium urocaniciphilum sp. nov., isolated from a wastewater treatment plant, and emended descriptions of Flavobacterium caeni and Flavobacterium terrigena. Int J Syst Evol Microbiol 64:1488–1494View ArticleGoogle Scholar
  12. Fukuda W, Kimura T, Araki S, Miyoshi Y, Atomi H, Imanaka T (2013) Lysobacter oligotrophicus sp. nov., isolated from an Antarctic freshwater lake in Antarctica. Int J Syst Evol Microbiol 63:3313–3318View ArticleGoogle Scholar
  13. Hashizume H, Igarashi M, Hattori S, Hori M, Hamada M, Takeuchi T (2001) Tripropeptins, novel antimicrobial agents produced by Lysobacter sp. I. Taxonomy, isolation and biological activities. J Antibiot 54:1054–1059View ArticleGoogle Scholar
  14. Hosoya S, Arunpairojana V, Suwannachart C, Kanjana-Opas A, Yokota A (2006) Aureispira marina gen. nov., sp. nov., a gliding, arachidonic acid-containing bacterium isolated from the southern coastline of Thailand. Int J Syst Evol Microbiol 56:2931–2935View ArticleGoogle Scholar
  15. Hosoya S, Arunpairojana V, Suwannachart C, Kanjana-Opas A, Yokota A (2007) Aureispira maritima sp. nov., isolated from marine barnacle debris. Int J Syst Evol Microbiol 57:1948–1951View ArticleGoogle Scholar
  16. Islam MT (2010) Mode of antagonism of a biocontrol bacterium Lysobacter sp. SB-K88 toward a damping-off pathogen Aphanomyces cochlioides. World J Microbiol Biotechnol 26:629–637View ArticleGoogle Scholar
  17. Jin Y, Kim YJ, Hoang VA, Jung SY, Nguyen NL, Min JW, Wang C, Yang DC (2014) Flavobacterium panaciterrae sp. nov., a β-glucosidase producing bacterium with ginsenoside-converting activity isolated from the soil of a ginseng field. J Gen Appl Microbiol 60:59–64View ArticleGoogle Scholar
  18. Johansen EJ, Nielsen P, Sjoholm C (1999) Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola, gen. nov., sp. nov. and reclassification of Cytophaga lytica to Cellulophaga lytica gen. nov., sp. comb. nov. Int J Syst Bacteriol 49:1231–1240View ArticleGoogle Scholar
  19. Kadouri D, O’Toole GA (2005) Susceptibility of biofilms to Bdellovibrio bacteriovorus attack. Appl Environ Microbiol 71:4044–4051View ArticleGoogle Scholar
  20. Kim SR, Kim YJ, Nguyen NL, Min JW, Jeon JN, Yang DU, Yang DC (2011) Flavobacterium ginsengiterrae sp. nov., isolated from a ginseng field. J Gen Appl Microbiol 57:341–346View ArticleGoogle Scholar
  21. Kim JJ, Kanaya E, Weon HY, Koga Y, Takano K, Dunfield PF, Kwon SW, Kanaya S (2012) Flavobacterium compostarboris sp. nov., isolated from leaf-and-branch compost, and emended descriptions of Flavobacterium hercynium, Flavobacterium resistens and Flavobacterium johnsoniae. Int J Syst Evol Microbiol 62:2018–2024View ArticleGoogle Scholar
  22. Kim JH, Choi BH, Jo M, Kim SC, Lee PC (2014) Flavobacterium faecale sp. nov., an agarase-producing species isolated from stools of Antarctic penguins. Int J Syst Evol Microbiol 64:2884–2890View ArticleGoogle Scholar
  23. Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, CambridgeView ArticleGoogle Scholar
  24. Kwon KK, Lee YK, Lee HK (2006) Costertonia aggregata gen. nov., sp. nov., a mesophilic marine bacterium of the family Flavobacteriaceae, isolated from a mature biofilm. Int J Syst Evol Microbiol 56:1349–1353View ArticleGoogle Scholar
  25. Lee K, Park SC, Yi H, Chun J (2013) Flavobacterium limnosediminis sp. nov., isolated from sediment of a freshwater lake. Int J Syst Evol Microbiol 63:4784–4789View ArticleGoogle Scholar
  26. Li S, Jochum CC, Yu F, Zaleta-Rivera K, Du L, Harris SD, Yuen GY (2008) An antibiotic complex from Lysobacter enzymogenes strain C3: antimicrobial activity and role in plant disease control. Phytopathology 98:695–701View ArticleGoogle Scholar
  27. Li A, Liu H, Sun B, Zhou Y, Xin Y (2014) Flavobacterium lacus sp. nov., isolated from a high-altitude lake, and emended description of Flavobacterium filum. Int J Syst Evol Microbiol 64:933–939View ArticleGoogle Scholar
  28. Liu H, Liu R, Yang SY, Gao WK, Zhang CX, Zhang KY, Lai R (2008) Flavobacterium anhuiense sp. nov., isolated from field soil. Int J Syst Evol Microbiol 58:756–760View ArticleGoogle Scholar
  29. Loch TP, Faisal M (2014) Flavobacterium spartansii sp. nov., a pathogen of fishes, and emended descriptions of Flavobacterium aquidurense and Flavobacterium araucananum. Int J Syst Evol Microbiol 64:406–412View ArticleGoogle Scholar
  30. Luo G, Shi Z, Wang G (2012) Lysobacter arseniciresistens sp. nov., an arsenite-resistant bacterium isolated from iron-mined soil. Int J Syst Evol Microbiol 62:1659–1665View ArticleGoogle Scholar
  31. O’Sullivan J, McCullough JE, Tymiak AA, Kirsch DR, Trejo WH, Principe PA (1988) Lysobactin, a novel antibacterial agent produced by Lysobacter sp. J Antibiot 51:1740–1744View ArticleGoogle Scholar
  32. Park JH, Kim R, Aslam Z, Jeon CO, Chung YR (2008) Lysobacter capsici sp. nov., with antimicrobial activity, isolated from the rhizosphere of pepper, and emended description of the genus Lysobacter. Int J Syst Evol Microbiol 58:387–392View ArticleGoogle Scholar
  33. Rickard AH, Stead AT, O’May GA, Lindsay S, Banner M, Handley PS, Gilbert P (2005) Adhaeribacter aquaticus gen. nov., sp. nov., a Gram negative isolate from a potable water biofilm. Int J Syst Evol Microbiol 55:821–829View ArticleGoogle Scholar
  34. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425Google Scholar
  35. Sangnoi Y, Sakulkeo O, Yuenyongsawad S, Kanjana-Opas A, Ingkaninan K, Plubrukarn A, Suwanborirux K (2008) Acetylcholinesterase-inhibiting activity of pyrrole derivatives from a novel marine gliding bacterium, Rapidithrix thailandica. Mar Drugs 6:578–586View ArticleGoogle Scholar
  36. Sangnoi Y, Srisukchayakul P, Arunpairojana V, Kanjana-Opas A (2009) Diversity of marine gliding bacteria in Thailand and their cytotoxicity. Electron J Biotechnol 12:1–8Google Scholar
  37. Sangnoi Y, Plubrukarn A, Arunpairojana V, Kanjana-Opas A (2014) A new antibacterial amino phenyl pyrrolidone derivative from a novel marine gliding bacterium Rapidithrix thailandica. World J Microbiol Biotechnol 30:1135–1139View ArticleGoogle Scholar
  38. Singh PD, Ward PC, Wells JS, Ricca CM, Trejo WH, Principe PA, Sykes RB (1982) Bacterial production of deacetoxycephalosporin C. J Antibiot 35:1397–1399View ArticleGoogle Scholar
  39. Spyere A, Rowley DC, Jensen PR, Fenical W (2003) New neoverrucosane diterpenoids produced by the marine gliding bacterium Saprospira grandis. J Nat Prod 66:818–822View ArticleGoogle Scholar
  40. Srinivasan S, Kim MK, Sathiyaraj G, Kim HB, Kim YJ, Yang DC (2010) Lysobacter soli sp. nov., isolated from soil of a ginseng field. Int J Syst Evol Microbiol 60:1543–1547View ArticleGoogle Scholar
  41. Srisukchayakul P, Suwannachart C, Sangnoi Y, Kanjana-Opas A, Hosoya S, Yokota A, Arunpairojana V (2007) Rapidithrix thailandica gen. nov., sp. nov., a marine gliding bacterium isolated from samples collected from the Andaman sea, along the southern coastline of Thailand. Int J Syst Evol Microbiol 57:2275–2279View ArticleGoogle Scholar
  42. Subhash Y, Sasikala Ch, Ramana ChV (2013) Flavobacterium aquaticum sp. nov., isolated from a water sample of a rice field. Int J Syst Evol Microbiol 63:3463–3469View ArticleGoogle Scholar
  43. Tamura K, Peterson D, Petersen N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739View ArticleGoogle Scholar
  44. Thomson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882View ArticleGoogle Scholar
  45. Vandecandelaere I, Segaert E, Mollica A, Faimali M, Vandamme P (2009) Phaeobacter caeruleus sp. nov., a blue-coloured, colony-forming bacterium isolated from a marine electroactive biofilm. Int J Syst Evol Microbiol 59:1209–1214View ArticleGoogle Scholar
  46. Verma DK, Rathore G (2013) Molecular characterization of Flavobacterium columnare isolated from a natural outbreak of columnaris disease in farmed fish, Catla catla from India. J Gen Appl Microbiol 59:417–424View ArticleGoogle Scholar
  47. Wang Y, Dai J, Zhang L, Luo X, Li Y, Chen G, Tang Y, Meng Y, Fang C (2009) Lysobacter ximonensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 59:786–789View ArticleGoogle Scholar
  48. Wonghirundecha S, Benjakul S, Sumpavapol P (2014) Total phenolic content, antioxidant and antimicrobial activities of stink bean (Parkia speciosa Hassk.) pod extracts. Songklanakarin J Sci Technol 36:301–308Google Scholar
  49. Xin YH, Liang ZH, Zhang DC, Liu HC, Zhang JL, Yu Y, Xu MS, Zhou PJ, Zhou YG (2009) Flavobacterium tiangeerense sp. nov., a cold-living bacterium isolated from a glacier. Int J Syst Evol Microbiol 59:2773–2777View ArticleGoogle Scholar
  50. Yagi H, Maruyama A (1999) A novel monoacyldiglycosyl-monoacylglycerol from Flavobacterium marinotypicum. J Nat Prod 62:631–632View ArticleGoogle Scholar
  51. Zhang L, Bai J, Wang Y, Wu GL, Dai J, Fang CX (2011) Lysobacter korlensis sp. nov. and Lysobacter bugurensis sp. nov., isolated from soil. Int J Syst Evol Microbiol 61:2259–2265View ArticleGoogle Scholar

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