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Int J Syst Evol Microbiol 57 (2007), 2874-2880; DOI  10.1099/ijs.0.65286-0
© 2007 International Union of Microbiological Societies

Pelagicoccus croceus sp. nov., a novel marine member of the family Puniceicoccaceae within the phylum ‘Verrucomicrobia’ isolated from seagrass

Jaewoo Yoon1, Naoya Oku2, Satoru Matsuda2, Hiroaki Kasai2 and Akira Yokota1

1 Institute of Molecular and Cellular Biosciences, The University of Tokyo, 1-1-1 Yayoi, Bunkyo-Ku, Tokyo 113-0032, Japan
2 Marine Biotechnology Institute Co. Ltd, 3-75-1, Heita, Kamaishi, Iwate 026-0001, Japan

Correspondence
Jaewoo Yoon
aa57058{at}mail.ecc.u-tokyo.ac.jp


   ABSTRACT
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An obligately aerobic, spherical, non-motile, pale-yellow pigmented bacterium was isolated from a piece of leaf of seagrass, Enhalus acoroides (L.f.) Royle, grown in Okinawa, Japan and was subjected to a polyphasic taxonomic study. Phylogenetic analyses based on 16S rRNA gene sequences revealed that the novel isolate N5FB36-5T shared approximately 96–98 % sequence similarity with the species of the genus Pelagicoccus of the family Puniceicoccaceae within the phylum ‘Verrucomicrobia’. The DNA–DNA relatedness values of strain N5FB36-5T with Pelagicoccus mobilis 02PA-Ca-133T and Pelagicoccus albus YM14-201T were below 70 %, which is accepted as the phylogenetic definition of a novel species. β-Lactam antibiotic susceptibility test and amino acid analysis of the cell wall hydrolysates indicated the absence of muramic acid and diaminopimelic acid in the cell walls, which suggested that this strain lacks an ordinary Gram-negative type of peptidoglycan in the cell wall. The DNA G+C content of strain N5FB36-5T was 51.6 mol%; MK-7 was the major menaquinone; and the presence of C16 : 0, C16 : 1{omega}7c and anteiso-C15 : 0 as the major cellular fatty acids supported the identification of the novel isolate as a member of the genus Pelagicoccus. On the basis of polyphasic taxonomic data, it was concluded that this strain should be classified as a novel species of the genus Pelagicoccus, for which the name Pelagicoccus croceus sp. nov. is proposed. The type strain is N5FB36-5T (=MBIC08282T=KCTC 12903T).

The GenBank/EMBL/DDBJ accession number for 16S rRNA gene sequence of strain N5FB36-5T is AB297922.


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The phylum ‘Verrucomicrobia’ (Hedlund et al., 1997Go; Hugenholtz et al., 1998Go) represents a well defined, major lineage within the domain Bacteria. A lot of culture-independent studies based on the 16S rRNA gene sequences revealed that this phylogenetic group is ubiquitous in nature (Hugenholtz et al., 1998Go; O'Farrell & Janssen, 1999Go; Joseph et al., 2003Go; Rappé & Giovannoni, 2003Go; Kanokratana et al., 2004Go; Haukka et al., 2005Go; Dedysh et al., 2006Go; Haukka et al., 2006Go). At present, it has been informally classified into five subdivisions numbered 1 to 5 (Hugenholtz et al., 1998Go) and has also been classified into six subdivisions numbered 1 to 6 (Vandekerckhove et al., 2000Go). Among them, subdivision 1 is equivalent to the family Verrucomicrobiaceae as described in the second edition of Bergey's Manual of Systematic Bacteriology (Garrity & Holt, 2001Go). In addition, recently, the class Opitutae, which is composed of two orders; the order Puniceicoccales containing the family Puniceicoccaceae and the order Opitutales containing the family Opitutaceae was recently proposed for classification of species belonging to subdivision 4 (Choo et al., 2007Go). Although verrucomicrobial 16S rRNA gene sequences have been identified from marine animals and plants (Weidner et al., 2000Go; Alain et al., 2002Go; Bowman & Nowak, 2004Go), only a few micro-organisms isolated from marine organisms within subdivisions 1 and 4 have been cultivated and validly reported (Scheuermayer et al., 2006Go; Choo et al., 2007Go; Kasai et al., 2007Go). However, owing to the problem of uncultivability, there are still only a few cultivated representatives so far and their ecological niche also remains to be elucidated.

As part of our programme to construct a comprehensive culture collection library of phylogenetically or functionally novel bacteria and fungi (http://www.nedo.go.jp/activities/portal/p02038.html), we have developed the in situ culture technique for the collection of yet-uncultured microbes from coastal waters (Yasumoto-Hirose et al., 2006Go). This new approach enabled us to discover a clustered set of novel marine verrucomicrobial species belonging to the class Opitutae (subdivision 4), for which we proposed a new genus Pelagicoccus (Yoon et al., 2007bGo). As another attempt towards the same mission, we designed a lectin-supplemented medium in the aim to collect bacteria in symbiotic associations with eukaryotes, which is based on the accumulating evidence that lectins are involved in many host–symbiont associations (Hirsch, 1999Go; Koike et al., 2004Go; McCowen et al., 1986Go; Venkataraman et al., 1997Go). Applications of this medium to the marine plant Enhalus acoroides (L.f.) Royle resulted in isolation of an additional novel species of the genus Pelagicoccus.

Strain N5FB36-5T was isolated in October 2005 from a piece of leaf of E. acoroides grown in the Kuira River mangrove estuary, Iriomotejima, Okinawa, Japan (GPS location; 2 ° 29.24' N, 12 ° 44.45' E). Isolation and enrichment of strain N5FB36-5T was performed on 1/10 strength marine agar 2216 (Difco) supplemented with 10 µg jack bean lectin concanavalin A (Wako) ml–1. To prepare this medium, 3.74 g marine broth 2216, 15 g agar, 250 ml artificial seawater (Lyman & Fleming, 1940Go) and 750 ml distilled water were mixed and autoclaved, after which a solution of 2.5 ml concanavalin A prepared at a concentration of 4 mg ml–1 in sterile distilled water was added, before the agar solidified. A piece of the freshly collected E. acoroides leaf (approx. 1 cm2) was vigorously crushed in 5 ml sterile artificial seawater with a glass rod and allowed to stand so that the solid particles could settle. The supernatant was further diluted to 10–1 dilution using sterile artificial seawater, of which 50 µl aliquot was spread on a 1/10 strength marine agar 2216 plate with concanavalin A. The enrichment agar medium was incubated for 2 months at room temperature. The resulting translucent colony was transferred twice on the same medium to purify the isolate and was used in this study. In the present study, we attempted to elucidate the phylogenetic position of strain N5FB36-5T using a polyphasic taxonomic approach, including 16S rRNA gene sequence analysis. In parallel, we performed physiological, biochemical and chemotaxonomic analyses to characterize the novel isolate. Based on these data, it is proposed that the isolate represents a novel species within the phylum ‘Verrucomicrobia’.

The temperature and pH range for growth were determined by incubating the isolates on the 1/5 strength marine agar 2216. The NaCl concentration for growth was determined in a salt tolerance test medium containing 1 % tryptone, 0.3 % yeast extract, 0.9 % MgCl2 . 6H2O, 0.9 % MgSO4 . 7H2O, 0.2 % CaCl2 . 2H2O, 0.06 % KCl and 1.5 % agar with 0–10 % (w/v) NaCl. Gram-staining was performed as described by Murray et al. (1994)Go. Cell morphology was observed using light microscopy (BX60; Olympus). The cells of strain N5FB36-5T on 1/5 strength marine agar 2216 were coccoid shaped ranging from 0.5 to 1.0 µm in diameter. Motility by flagellum and gliding movement were not seen. Cell divisions by binary fission were observed. Growth under anaerobic conditions was determined after 2 weeks of incubation in an AnaeroPack (Mitsubishi Gas Chemical) on 1/5 strength marine agar 2216. Catalase activity was determined by bubble formation in a 3 % H2O2 solution. Oxidase activity was determined by cytochrome oxidase paper (Nissui Pharmaceutical). API 20E, API 50CH and API ZYM strips (bioMérieux) were used to determine physiological and biochemical characteristics. API 20E, API 50CH and API ZYM were read after 72 h incubation at 30 °C and 4 h incubation at 37 °C, respectively. Determination of the respiratory quinone system and cellular fatty acid composition was carried out as described previously (Katsuta et al., 2005Go). DNA was prepared according to the method of Marmur (1961)Go from cells grown on 1/5 strength marine agar 2216 and the DNA base composition was determined by using the HPLC method of Mesbah et al. (1989)Go. DNA–DNA hybridizations were carried out with photobiotin-labelled probes in microplate wells as described by Ezaki et al. (1989)Go. The hybridization temperature was set at 48 °C. Hybridization was performed using five replications for each. Of the values obtained, the highest and lowest for each sample were excluded and the mean of the remaining three values is quoted as the DNA–DNA relatedness value. β-Lactam antibiotic susceptibility test against the novel isolate was checked on 1/5 strength marine agar 2216, using 8 mm paper disc (Advantec) at the following antibiotic concentrations: 1, 10, 100, 500 and 1000 µg ml–1 ampicillin and 1, 10, 100, 500 and 1000 µg ml–1 penicillin G. Cell walls were prepared by the methods described by Schleifer & Kandler (1972)Go, and amino acids in an acid hydrolysate of the cell walls were identified by TLC (Harper & Davis, 1979Go) and HPLC, as their phenylthiocarbamoyl derivatives, with a model LC-10AD HPLC apparatus (Shimazu) equipped with a Wakopak WS-PTC column (Wako Pure Chemical Industries) (Yokota et al., 1993Go). An approximately 1500 bp fragment of the 16S rRNA gene was amplified from the extracted DNA by using bacterial universal primers specific to the 16S rRNA gene: 27F and 1492R (Escherichia coli numbering system; Weisburg et al., 1991Go). To ascertain the phylogenetic position of the novel isolate, the 16S rRNA gene sequence of strain N5FB36-5T was compared with the sequences obtained from GenBank (National Center for Biotechnology Information, http://www.ncbi.nlm.nih.gov). Multiple alignments of the sequences were performed using CLUSTAL_X (version 1.83) (Thompson et al., 1997Go). Alignment gaps and ambiguous bases were not taken into consideration when the 1187 bases of the 16S rRNA gene nucleotides were compared. The phylogenetic relationships were determined by using the maximum-likelihood method (Felsenstein, 1985Go) and the Ratchet model (Sikes & Lewis, 2001Go) of evolution in PAUP* 4.0b10 (Swofford, 2002Go). Bootstrap analysis was performed by using 1000 trial replications to provide confidence estimates for tree topologies. The similarity values were calculated using the MEGA 3.1 software (Kumar et al., 2004Go).

An evolutionary tree based on the maximum-likelihood method generated a comparison of the 16S rRNA gene sequences and revealed that strain N5FB36-5T was phylogenetically affiliated with the Pelagicoccus species of the family Puniceicoccaceae belonging to the order Puniceicoccales within the phylum ‘Verrucomicrobia’ with a bootstrap confidence value of 100 % (Fig. 1Go). Comparative analysis of the 16S rRNA gene sequences revealed that the sequence of strain N5FB36-5T had a similarity of 98.7 % to that of Pelagicoccus mobilis 02PA-Ca-133T, 97.9 % to Pelagicoccus albus YM14-201T and 96.8 % to the three strains (H-MN57T, H-MN48 and MN1-156) of Pelagicoccus litoralis. All other cultivated species of the class Opitutae (subdivision 4) with currently published names were more distantly related, showing a 16S rRNA gene sequence similarity of less than 90 %.


Figure 1
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  		Fig. 1. Maximum-likelihood phylogenetic tree showing the position of strain N5FB36-5T. Numbers at branch nodes are bootstrap values based on 1000 replications. The sequence determined in this study is shown in bold. The sequence of Escherichia coli ATCC 11775T was used as the outgroup reference. Subdivisions of the phylum ‘Verrucomicrobia’ are shown as SD 1–6. Bar, 0.1 substitutions per site.

 
DNA–DNA hybridization values between strain N5FB36-5T and Pelagicoccus mobilis 02PA-Ca-133T and Pelagicoccus albus YM14-201T were 1.4 and 2.2 %, respectively. These results strongly suggest that strain N5FB36-5T should be classified as a separate species, if it can be distinguished by phenotypic traits (Wayne et al., 1987Go).

As shown in Table 1Go, the predominant cellular fatty acids of five novel strains were C15 : 0 (21.2 %), C16 : 0 (20.7 %), C16 : 1{omega}7c (12.7 %) and anteiso-C15 : 0 (25.4 %), which are similar to other members of the genus Pelagicoccus. On the other hand, strain N5FB36-5T is distinguished from the other species of the genus Pelagicoccus by a different proportion of C15 : 0. Furthermore, on the basis of their fatty acid composition, this strain is differentiated from Coraliomargarita akajimensis 04OKA010-24T, Cerasicoccus arenae YM26-026T and Puniceicoccus vermicola IMCC1545T, their phylogenetically neighbouring taxa, indicating that strain N5FB36-5T probably represents an independent species of the genus Pelagicoccus of the family Puniceicoccaceae within the phylum ‘Verrucomicrobia’.


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  		Table 1. Cellular fatty acid content (%) of Pelagicoccus croceus sp. nov. and the related taxa of the family Puniceicoccaceae

Taxa: 1, strain N5FB36-5T; 2, Pelagicoccus mobilis 02PA-Ca-133T (data from Yoon et al., 2007bGo); 3, Pelagicoccus albus YM14-201T (Yoon et al., 2007bGo); 4, Pelagicoccus litoralis H-MN57T (Yoon et al., 2007bGo); 5, Coraliomargarita akajimensis 04OKA010-24T (Yoon et al., 2007aGo); 6, Cerasicoccus arenae YM26-026T (Yoon et al., 2007cGo); 7, Puniceicoccus vermicola IMCC1545T (Choo et al., 2007Go). Data are expressed as percentages of total fatty acids. Fatty acids representing less than 1 % are not shown. –, Not detected; ND, not described; tr, trace.

 
When the isolate was grown in the presence of increasing concentrations (1–1000 µg ml–1) of β-lactam antibiotics, it showed a remarkable resistance to ampicillin and penicillin G. The cell wall was prepared by disrupting cells, followed by heating with 3 % SDS, washing and centrifugation. Amino acid analysis of the cell wall hydrolysate indicated the absence of muramic acid and diaminopimelic acid in the cell wall, suggesting that the strain does not contain an ordinary Gram-negative type of peptidoglycan in the cell walls. This taxonomic trait, consistently observed in all verrucomicrobial species within the class Opitutae (subdivision 4), is relevant to parasitic bacteria such as mycoplasma and chlamydia. Although the natural habitat of Pelagicoccus has not been specified yet, it is quite possible that they are symbionts of certain marine eukaryotic hosts in at least some parts of their life history. This speculation is supported by the recent reports that both maternally inherited cytoplasmic endosymbionts in nematodes of the genus Xiphinema and defensive extrusive ectosymbionts on hypotrich ciliates were identified as novel groups of the phylum ‘Verrucomicrobia’ (Petroni et al., 2000Go; Vandekerckhove et al., 2000Go).

Strain N5FB36-5T also showed distinct phenotypic features that discriminated it from the cultivated members of the class Opitutae given in Table 2Go.


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  		Table 2. Differential phenotypic characteristics of Pelagicoccus croceus sp. nov. and the related genera of the class Opitutae within the phylum ‘Verrucomicrobia’

Taxa: 1, strain N5FB36-5T; 2, Pelagicoccus mobilis 02PA-Ca-133T (data from Yoon et al., 2007bGo); 3, Pelagicoccus albus YM14-201T (Yoon et al., 2007bGo); 4, Pelagicoccus litoralis H-MN57T (Yoon et al., 2007bGo); 5, Coraliomargarita akajimensis 04OKA010-24T (Yoon et al., 2007aGo); 6, Cerasicoccus arenae YM26-026T (Yoon et al., 2007cGo); 7, Puniceicoccus vermicola IMCC1545T (Choo et al., 2007Go); 8, Alterococcus agarolyticus BCRC 19135T (Shieh & Jean, 1998Go); 9, Opitutus terrae DSM 11246T (Chin et al., 2001Go). +, Positive; W, weakly positive; –, negative; ND, no data.

 
Based on the results of the phylogenetic analysis and its biochemical and physiological properties, strain N5FB36-5T isolated from a piece of leaf of seagrass E. acoroides should be classified as a novel species of the genus Pelagicoccus of the family Puniceicoccaceae within the phylum ‘Verrucomicrobia’, for which the name Pelagicoccus croceus sp. nov. is proposed.

Description of Pelagicoccus croceus sp. nov.
Pelagicoccus croceus (cro.ce'us. L. masc. adj. croceus, saffron-coloured, yellow, golden, referring to the pale-yellow colour of colonies).

Cells are obligately aerobic, non-motile, cocci 0.5–1.0 µm in diameter. Neither cellular gliding movement nor swarming growth is observed. Colonies grown on 1/5 strength marine agar 2216 are circular, convex and pale-yellow. The temperature range for growth is 20–30 °C, optimally at 25–30 °C, but no growth occurs at 4 or 45 °C. The pH range for growth is 6.5–9.0. NaCl is required for growth and cells can tolerate up to 5 % (w/v). Growth occurs in the presence of ampicillin (1–1000 µg ml–1) and penicillin G (1–1000 µg ml–1). Catalase- and oxidase-positive. Nitrate is not reduced. Aesculin is hydrolysed but agar, DNA, starch, gelatin and urea are not. The reaction for ONPG is positive, but acetoin, tryptophan deaminase, citrate utilization, arginine dihydrolase, lysine decarboxylase, ornithine decarboxylase, hydrogen sulfide and indole production are negative. Acid is produced from methyl β-D-xylopyranoside, methyl {alpha}-D-mannnopyranoside, aesculin ferric citrate, lactose, melibiose, D-turanose, D-lyxose, D-tagatose and 5-ketogluconate, but not from sucrose, glycerol, galactose, fructose, mannose, mannitol, sorbitol, trehalose, D-fucose, L-fucose, D-arabitol, L-arabitol, erythritol, D-arabinose, L-arabinose, ribose, D-xylose, L-xylose, adonitol, glucose, sorbose, rhamnose, dulcitol, inositol, methyl {alpha}-D-glucopyranoside, N-acetyl-D-glucosamine, amygdalin, arbutin, salicin, cellobiose, maltose, inulin, melezitose, raffinose, starch, glycogen, xylitol, gentiobiose, gluconate or 2-ketogluconate. Alkaline phosphatase, leucine arylamidase and acid phosphatase are positive, but β-galactosidase, naphthol-AS-BI-phosphohydrolase, {alpha}-galactosidase, {alpha}-glucosidase, valine arylamidase, trypsin, esterase (C4), esterase lipase (C8), lipase (C4), cystine arylamidase, chymotrypsin, β-glucuronidase, β-glucosidase, N-acetyl-β-glucosaminidase, {alpha}-mannosidase and {alpha}-fucosidase are negative. The usual components of bacterial cell walls such as muramic acid and diaminopimelic acid could not be detected. Major fatty acid components (>1.0 %) include C14 : 0 (1.3 %), C15 : 0 (21.2 %), C16 : 0 (20.7 %), C17 : 0 (6.8 %), C15 : 1{omega}6c (2.6 %), C16 : 1{omega}7c (12.7 %), C18 : 1{omega}9c (1.5 %), iso-C16 : 0 (1.8 %), anteiso-C15 : 0 (25.4 %) and anteiso-C17 : 0 (1.5 %). The G+C content of DNA is 51.6 mol%.

The type strain, N5FB36-5T (=MBIC08282T=KCTC 12903T), was isolated from the leaf surface of seagrass E. acoroides (L.f.) Royle.


   ACKNOWLEDGEMENTS
 
We thank Sachiko Kawasaki, Atsuko Katsuta, Ayako Matsuzaki, Tomomi Haga and Yukiko Itazawa for their technical assistance. This work was supported by the New Energy and Industrial Technology Development Organization (NEDO).


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