SGM Journals
Proteobacteria

Photobacterium jeanii sp. nov., isolated from corals and zoanthids

Luciane A. Chimetto, Ilse Cleenwerck, Cristiane C. Thompson, Marcelo Brocchi, Anne Willems, Paul De Vos, Fabiano L. Thompson

  • 1Department of Genetics, Evolution and Bioagents, Institute of Biology, State University of Campinas (UNICAMP), Campinas, São Paulo, Brazil
  • 2Department of Genetics, Institute of Biology, Federal University of Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil
  • 3BCCM/LMG Bacteria Collection, Ghent University, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium
  • 4Microbial Genetics Laboratory, FIOCRUZ-IOC, Oswaldo Cruz Foundation, Rio de Janeiro, Brazil
  • 5Laboratory of Microbiology, Faculty of Sciences, Ghent University, K. L. Ledeganckstraat 35, B-9000 Ghent, Belgium
  • Correspondence
    Fabiano L. Thompson
    fabiano.thompson{at}biologia.ufrj.br

    • International Journal of Systematic and Evolutionary Microbiology 2010; 60(12):2843–2848 · https://doi.org/10.1099/ijs.0.019968-0

    View at publisher PubMed

    Abstract

    Four novel isolates (R-40508T, R-40507, R-40903 and R-21419) were obtained from different cnidarian species (Phyllogorgia dilatata, Merulina ampliata and Palythoa caribaeorum) from different places in Brazil and Australia. The novel isolates formed a tight phylogenetic group based on 16S rRNA, recA, topA, ftsZ, mreB and rpoA gene sequences. Their closest phylogenetic neighbours were the type strains of Photobacterium leiognathi, P. rosenbergii and P. halotolerans, sharing 97.1–97.5 % 16S rRNA gene sequence similarity. DNA–DNA hybridization between a representative strain (R-40508T) and the type strains of these Photobacterium species revealed less than 20 % relatedness, showing that the new isolates belong to a novel species. Several phenotypic features allow the differentiation of the novel species from its closest phylogenetic neighbours. It has gelatinase and lipase activity and can utilize melibiose, but it cannot grow on 6 % NaCl. In addition, the novel species has the fatty acid iso-C16 : 0, but lacks the fatty acids C17 : 0, C17 : 0 cyclo, iso-C17 : 0, C17 : 1ω8c and iso-C17 : 1ω9c. The name Photobacterium jeanii sp. nov. is proposed for this species, with the type strain R-40508T (=LMG 25436T =CAIM 1817T). The G+C content of the type strain is 45.5 mol%.

    • The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA, recA, topA, ftsZ, mreB and rpoA gene sequences of strains of Photobacterium jeanii sp. nov. are GU065209–GU065227 and AJ842701, as detailed in Supplementary Table S1.

    • Details of sequence accession numbers and strain-dependent phenotypic properties are available as supplementary material with the online version of this paper.

    There has been growing interest in coral microbiology in recent years, particularly because of increasing awareness of the role of corals in the marine environment and their extinction (Rohwer et al., 2001; Dinsdale et al., 2008; Sussman et al., 2009; Shnit-Orland & Kushmaro, 2009). One of the main causes of coral extinction seems to be infectious disease, caused mainly by vibrios (Rosenberg et al., 2007). Coral bacteria may also have a positive effect on the coral holobiont. Bacteria living in the coral mucus and tissue may be a first line of defence for their holobiont hosts, protecting them against disease (Ritchie, 2006). Photobacterium species associated with corals have been shown to be able to produce antibiotics that would protect the coral holobiont or would allow a competitive advantage (Ritchie, 2006). Other beneficial effects on the coral holobiont may include nitrogen fixation (Chimetto et al., 2008), provision of a food resource (Kooperman et al., 2007) and chitin decomposition (Ducklow & Mitchell, 1979). Photobacterium rosenbergii was one of the recently described species associated with healthy and diseased corals in Australia (Thompson et al., 2005a). This species has also been found in association with healthy and diseased corals in Brazil (Chimetto et al., 2009).

    In the present study, a detailed polyphasic taxonomic analysis was performed on four novel isolates obtained in different studies in order to determine their exact taxonomic position (Table 1⇓). They appeared to be related to Photobacterium species on the basis of 16S rRNA gene sequence analysis (Alves et al., 2010; Chimetto et al., 2009; Thompson et al., 2005b).

    Table 1.

    Strains of Photobacterium jeanii sp. nov

    All isolates were obtained using marine agar (MA) at 28 °C after 48 h of incubation. Sequences of the 16S rRNA gene and genes encoding a recombination repair protein (recA), topoisomerase I (topA), a cell-division protein (ftsZ), an actin-like cytoskeleton protein (mreB) and the RNA polymerase alpha subunit (rpoA) were obtained as described previously (Chimetto et al., 2008, 2009). Primers used for gene amplification and sequencing are described in Thompson et al. (2001b, 2005b) and Sawabe et al. (2007). Raw sequence data were transferred to ChromasPro version 1.34 (), where consensus sequences were determined. Pairwise similarities of these sequences with sequences from the EMBL database were calculated with the BioNumerics 4.5 software package (Applied Maths) using an open gap penalty of 100 % and a unit gap penalty of 0 %. Sequences were aligned using clustal w. Similarity matrices and phylogenetic trees were constructed using the mega version 4.0 software (Tamura et al., 2007) and BioNumerics 4.5 software (Applied Maths). Trees were drawn using the neighbour-joining (Saitou & Nei, 1987) and maximum-parsimony (Eck & Dayhoff, 1966) methods. The robustness of each topology was checked by 1000 bootstrap replications (Felsenstein, 1985). The gene sequence data obtained in this study are available through the open-access website taxvibrio (). The GenBank accession numbers for the 16S rRNA, ftsZ, mreB, recA, rpoA and topA gene sequences determined in this study are listed in Supplementary Table S1, available in IJSEM Online. DNA–DNA hybridization (DDH) experiments were performed using Ezaki's microplate method as described in detail previously (Ezaki et al., 1989; Willems et al., 2001). Hybridization was conducted at 40 °C in the presence of 50 % formamide. Reciprocal reactions were performed for every DNA pair and their variation was within the limits of this method (Goris et al., 1998). The G+C content of the DNAs was determined using HPLC, as described previously (Mesbah et al., 1989). Analysis of fatty acid methyl esters was carried out as described by Huys et al. (1994). For fatty acid analysis, cells were grown on TSA (Difco) supplemented with 2 % NaCl for 24 h at 28 °C. Phenotypic characterization was performed as described previously (Thompson et al., 2001a, 2006). Type strains of known Photobacterium species were included in these analyses as positive controls.

    16S rRNA gene sequence analysis revealed that the four isolates formed a tight monophyletic group affiliated to the genus Photobacterium (Fig. 1⇓). The four novel isolates formed a tight cluster with more than 99 % 16S rRNA gene sequence similarity. The closest neighbours of the novel isolates were the type strains of Photobacterium leiognathi (97.4 % sequence similarity), P. rosenbergii and P. halotolerans (both 97.1 % sequence similarity), P. lutimaris and P. angustum (both 97.0 % similarity). The 16S rRNA gene sequence similarity towards other Photobacterium species with validly published names was below 96.5 %. Phylogenetic analysis based on 16S rRNA, recA, topA, ftsZ, mreB and rpoA gene sequences (4949 nt in total) confirmed that the isolates form a tight group related to P. rosenbergii (Fig. 2⇓). The novel isolates shared less than 95 % concatenated gene sequence similarity with their closest neighbour, indicating clearly that they belong to a novel Photobacterium species.

    Figure image not available in archive
    Fig. 1.

    Neighbour-joining phylogenetic tree of Photobacterium species based on 16S rRNA gene sequences (1466 nt) showing the position of the novel strains (Photobacterium jeanii sp. nov.). The optimal tree with the sum of branch lengths of 0.30919266 is shown. Evolutionary distances were computed using the Jukes–Cantor method. All positions containing alignment gaps and missing data were eliminated only in pairwise sequence comparisons (pairwise deletion option). Phylogenetic analyses were conducted in mega4. Bootstrap values (>50 %) based on 1000 resamplings are shown. Vibrio cholerae ATCC 14035T was used as an outgroup. Bar, 1 % estimated sequence divergence.

    Figure image not available in archive
    Fig. 2.

    Neighbour-joining phylogenetic tree based on concatenated 16S rRNA, ftsZ, mreB, recA, rpoA and topA gene sequences (4949 nt) showing the position of the novel strains (P. jeanii sp. nov.). Evolutionary distances were computed using the Jukes–Cantor method. Codon positions included were first+second+third+non-coding. All positions containing alignment gaps and missing data were eliminated only in pairwise sequence comparisons (pairwise deletion option). Phylogenetic analyses were conducted in mega4. Bootstrap values (>50 %) based on 1000 resamplings are shown for the neighbour-joining/maximum-parsimony methods. Campylobacter jejuni NCTC 11168T was used as an outgroup. Bar, 5 % estimated sequence divergence.

    DDH experiments were performed with all four isolates and the type strains of the closest phylogenetic neighbours. Relatedness between the novel isolates varied between 84 and 97 %, showing that they belong to a single species. The novel isolate R-40508T had only 19, 15, 11 and 9 % DDH relatedness with P. lutimaris LMG 25278T, P. rosenbergii LMG 22223T, P. leiognathi LMG 4228T and P. halotolerans LMG 22194T, respectively. Standard deviations of all hybridization experiments were below 10 %. Clearly, the DDH data demonstrate that the four isolates represent a novel species of the genus Photobacterium.

    Several phenotypic features can be used to differentiate the novel species from its closest phylogenetic neighbours. The novel species has gelatinase and lipase activity and it can ferment melibiose, but it cannot grow on 6 % NaCl (Table 2⇓). In addition, the novel species lacks the fatty acids C17 : 0, C17 : 0 cyclo, iso-C17 : 0, C17 : 1ω8c and iso-C17 : 1ω9c, which are commonly found in Photobacterium and Vibrio species (Table 3⇓). For instance, iso-C17 : 0 is found in P. leiognathi, P. rosenbergii and P. lutimaris, whereas C17 : 0 is found in P. leiognathi and P. halotolerans. Phenotypic and chemotaxonomic variation was observed among the strains of the novel species, suggesting a good representation of the phenotype of the novel group (Supplementary Table S2). Based on the polyphasic analysis presented in this study, we propose to classify the four isolates in the novel species Photobacterium jeanii sp. nov. Another species of the genus has been described as ‘Photobacterium swingsii’ (Gomez-Gil et al., 2011), although the paper describing this organism is currently in press and the name has not yet been validly published, hence our use of a first name in forming the epithet.

    Table 2.

    Phenotypic differences between P. jeanii sp. nov. and related Photobacterium species

    Strains/species: 1, P. jeanii sp. nov. (four strains); 2, P. leiognathi (unless indicated, data from Baumann & Baumann, 1984; Nogi et al., 1998); 3, P. rosenbergii (Thompson et al., 2005a); 4, P. lutimaris (Jung et al., 2007); 5, P. halotolerans (Rivas et al., 2006); 6, P. ganghwense FR1311T (Park et al., 2006); 7, P. lipolyticum KCTC 10562T (Yoon et al., 2005); 8, P. phosphoreum LMG 4233T (Nogi et al., 1998; Ast et al., 2007; Yoshizawa et al., 2009); 9, P. angustum CIP 75.10T (Baumann & Baumann, 1984; Nogi et al., 1998; Yoshizawa et al., 2009); 10, P. aquimaris LC2-065T (Yoshizawa et al., 2009); 11, P. indicum LMG 22857T (Xie & Yokota, 2004; Ast et al., 2007); 12, P. profundum (Nogi et al., 1998). +, Positive; −, negative; w, weak; v, variable; nd, no data available. All taxa are negative for Gram stain and lysine and ornithine decarboxylases. Data in parentheses are for type strains.

    Table 3.

    Cellular fatty acid contents of the novel isolates (P. jeanii sp. nov.) and related taxa of the genus Photobacterium

    Strains: 1, P. jeanii sp. nov. R-40508T, R-40507, R-40903 and R-21419 (range of values); 2, P. leiognathi LMG 4228T; 3, P. rosenbergii LMG 22223T; 4, P. lutimaris LMG 25278T; 5, P. halotolerans LMG 22194T. Data were obtained in this study and are expressed as percentages of total fatty acids. Fatty acids representing <1 % in all strains are not shown; −, not detected or <1 %.

    Description of Photobacterium jeanii sp. nov.

    Photobacterium jeanii (jea′ni.i. N.L. gen. n. jeanii of Jean, after the Belgian microbiologist Jean Swings).

    Colonies are convex, round (1 mm in diameter), beige and opaque with entire and smooth margins after 2 days at 28 °C on MA. Cells are small coccobacilli, Gram-negative, motile and catalase- and oxidase-positive, 2–2.5 μm long and 1–2 μm wide after 1 day at 28 °C on MA. Green colonies with poor growth appear on the selective medium TCBS. Prolific growth occurs between 20 and 35 °C and at NaCl concentrations of 0.5–2 % (w/v) in TSA. No growth appears at 4, 7 or 42 °C or in 0 or 6 % NaCl. Positive for alkaline phosphatase, esterase (C4), esterase lipase (C8), lipase (C14), leucine arylamidase, valine arylamidase (weak reaction), trypsin, acid phosphatase, naphthol-AS-BI-phosphohydrolase, β-galactosidase (except R-40903), α-glucosidase, N-acetyl-β-glucosaminidase (except R-21419 and R-40508T), arginine dihydrolase, acetoin production (weak for R-40508T and R-40903) and gelatinase. Cells ferment glucose, melibiose and sucrose (except R-40507 and R-40903) and reduce nitrate to nitrite. Cystine arylamidase, α-chymotrypsin, α-galactosidase, β-glucuronidase, β-glucosidase, α-mannosidase, α-fucosidase, lysine decarboxylase, ornithine decarboxylase, urease and tryptophan deaminase activities are absent. Citrate is not utilized and H2S and indole are not produced. Mannitol (except R-40903), inositol, sorbitol, rhamnose, amygdalin and arabinose are not fermented. The DNA G+C content of the type strain is 44.5 mol%. The most abundant cellular fatty acids are summed feature 3 (iso-C15 : 0 2-OH and/or C16 : 1ω7c), C16 : 0, C18 : 1ω7c and C18 : 1ω6c. The following fatty acids are detected in small amounts: C14 : 0, iso-C16 : 0, C12 : 0, C12 : 0 3-OH, summed feature 2 (C14 : 0 3-OH and/or iso-C16 : 1 I, an unidentified fatty acid with an equivalent chain-length of 10.928 and/or C12 : 0 ALDE) and iso-C15 : 0.

    The type strain is R-40508T (=LMG 25436T =CAIM 1817T), isolated from mucus of the zoanthid Palythoa caribaeorum in the São Sebastião channel, Brazil.

    Acknowledgments

    The authors acknowledge grants from FAPERJ, FAPESP, CNPq and IFS. The BCCM/LMG Bacteria Collection is supported by the Federal Public Planning Service-Science Policy, Belgium. L. A. C. acknowledges a PhD scholarship provided by CNPq, the BCCM/LMG Bacteria Collection for providing reference strains and technical support and Colin Munn for his permission to use strain R-21419. We thank Katrien Engelbeen (BCCM/LMG), Stefanie Van Trappen (BCCM/LMG), Alvaro Migotto (CEBIMAR-USP) and Bruno Gomez-Gil (CIAD) for technical assistance and valuable comments.

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