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Alteromonas Hispanica Sp. Nov., a Polyunsaturated-Fatty-Acid-Producing

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Alteromonas Hispanica Sp. Nov., a Polyunsaturated-Fatty-Acid-Producing 1 Alteromonas hispanica sp. nov., a polyunsaturated-fatty-acid-producing, 2 halophilic bacterium isolated from Fuente de Piedra (S.E., Spain) 3 4 Fernando Martínez-Checa, Victoria Béjar, Inmaculada Llamas, Ana del Moral 5 and Emilia Quesada. 6 7 Microbial Exopolysaccharide Research Group, Department of Microbiology, 8 Faculty of Pharmacy, Cartuja Campus, University of Granada, 18071 Granada, 9 Spain. 10 11 Key words: Alteromonas, Alteromonas hispanica, halophiles, 12 exopolysaccharides, polyunsaturated fatty acids. 13 14 Subject category: taxonomic note, new taxa, γ-Proteobacteria. 15 16 Author for correspondence: E. Quesada, Department of Microbiology, Faculty of 17 Pharmacy, Cartuja Campus, University of Granada, 18071 Granada, Spain. 18 Tel: +34 958 243871 19 Fax: +34 958 246235 20 e-mail: [email protected] 21 22 The GenBank/EMB/DDBJ accession number for the 16S rRNA gene sequence 23 of strain Alteromonas hispanica F-32T is AY926460. 1 1 Abstract 2 3 Strain F-32T, which produces exopolysaccharides and contains polyunsaturated 4 fatty acids, was isolated from a hypersaline water sample collected from Fuente 5 de Piedra (S.E. Spain). Phylogenetic analyses indicated conclusively that the 6 strain in question belonged to the genus Alteromonas. Phenotypic tests showed 7 that it could be assigned to the genus Alteromonas although it had a number of 8 distinctive characteristics; it is moderately halophilic, growing best with 7.5 -10% o 9 w/v NaCl; it grows at 4 C and produces H2S; it does not grow with D-cellobiose, 10 D-fructose, D-galactose, D-glucose or lactose as sole sources of carbon and 11 energy; its fatty-acid profile is typical of Alteromonas but it also contains a large 12 amount of an unusual acid with three double bonds (18:3 ω6c [6, 9, 12]; 5.01%, 13 w/v). The major isoprenoid quinone is Q8. The DNA G+C composition is 46.3 14 mol%. The phylogenetic, phenotypic and genetic properties of strain F32T place 15 it within a novel species, for which we propose the name Alteromonas hispanica 16 sp. nov. The type strain is F-32T (= CECT 7067T = LMG 22958T). 17 18 2 1 The genus Alteromonas was isolated and named by Baumann et al. (1972) 2 (emended description by Gauthier et al., 1995; and later Van Trappen et al., 3 2004) and originally contained a phylogenetically and phenotypically 4 heterogeneous group of Gram-negative, heterotrophic, marine bacteria, motile 5 by a single polar flagellum. Many of its species, however, have gradually been 6 reclassified into other genera such as Marinomonas, Pseudoalteromonas, and 7 Shewanella (Van Landschoot & de Ley, 1983; MacDonnell & Colwell, 1985; 8 Coyne et al., 1989; Gauthier et al., 1995; Sawabe et al., 2000; Ivanova et al., 9 2000; 2001). Nowadays Alteromonas comprises only four valid species: A. 10 macleodii (Baumann et al., 1972 and 1984; Gauthier et al., 1995; Yi et al., 11 2004), A. marina (Yoon et al., 2003), A. stellipolaris (Van Trappen et al., 2004) 12 and A. litorea (Yoon et al., 2004). Together with the genus Glaciecola (Bowman 13 et al., 1998) and Aestuariibacter (Yi et al., 2004), it is included within the family 14 Alteromonadaceae (Ivanova et al., 2004). 15 16 Alteromonadaceae are Gram-negative, rod-shaped, motile bacteria that 17 do not form endospores or microcysts. They are chemo-organotrophs, have a 18 respiratory metabolism and use oxygen as electron acceptor. They do not 19 denitrify or have dihydrolase activity. All the species require Na+ for growth and 20 in most of them the major isoprenoid quinone is Q8. The major fatty acids are 21 16:0, 16:1 ω7c, and 18:1 ω7c. All the species have been isolated from marine 22 habitats (coastal sea waters and marine invertebrates). The family is a member 23 of the γ-proteobacteria with the following nucleotide sequence characteristics: 24 304 (A), 734 (A), 736 (T), 770 (T), 809 (A). The type genus is Alteromonas 25 (Ivanova et al., 2004). 3 1 Van Trappen et al. (2004) made the last emended description of 2 Alteromonas, which was based on Gauthier et al (1995), when they discovered 3 that members of the genus were prosthecate, budding bacteria. In addition to 4 the traits reported for the family, the genus also includes bacteria which are 5 catalase and oxidase positive, unpigmented and not luminescent. Species of 6 the genus do not usually grow at 4oC, do not accumulate poly-β- 7 hydroxybutyrate and require a sea-water base for growth but not organic growth 8 factors. A. macleodii, A. marina and A. stellipolaris produce buds and prostheca 9 when they grow at low temperatures (12º - 20oC) for 3 or more days in complex 10 media with added sea salts. The G+C content of the DNA is 44 to 47 mol%. The 11 type species is A. macleodii. 12 13 In this study we describe strain F32T of Alteromonas, for which we 14 propose the name Alteromonas hispanica. This strain is the only representative 15 of the genus Alteromonas identified so far that has been isolated from an inland 16 hypersaline habitat and produces polyunsaturated fatty acids (PUFAs) at a 17 relatively high incubation temperature (32oC), which contradicts the notion that 18 only barophilic and psychrophilic marine species are able to produce significant 19 levels of PUFAs (Nogi et al., 1998; Russell and Nichols, 1999). 20 21 The strain studied here was isolated in 1998 from a hypersaline water sample 22 taken from Fuente de Piedra (Málaga, S. Spain), an inland, hypersaline 23 wetland, during a wide research program aimed at discovering new halophilic 24 bacteria for biotechnological purposes (Martínez-Cánovas et al., 2004; 25 Quesada et al., 2004). Strain F-32T was isolated using MY medium (Moraine & 4 1 Rogovin 1966), supplemented with 10% w/v marine salts (Rodriguez-Valera et 2 al., 1981). The strain was kept and routinely grown in MY medium, with the 3 addition of 7.5% w/v marine salts for optimum growth. Strain F32T was originally 4 characterized phenotypically by Martínez-Cánovas et al. (2004) by means of 5 135 tests. Its flagellation pattern was determined in this work by transmission 6 electron microscopy of negatively stained cells. The phenotypic data are given 7 in the species description. Table 1 shows the main phenotypic differences 8 between strain F-32T and the other four species of the genus Alteromonas. The 9 same table contains the G+C content of strain F32T estimated from the midpoint 10 value (Tm) of the DNA thermal denaturation profile, as described in Martínez- 11 Cánovas et al. (2004). 12 13 Colonies used for the analysis of prostheca and buds were grown on MY (7.5% 14 w/v) for 7 days at 12oC, as recommended by Van Trappen et al. (2004). EPS 15 and poly-β-hydroxybutyrate granules were observed in cells grown on the same 16 medium after 1 day’s incubation at 32oC. Transmission electron micrographs 17 were taken using the methods described by Bouchotroch et al. (2001). 18 19 Phylogenetic analyses were made according to Bouchotroch et al. (2001). We 20 determined the near complete 16S rRNA gene sequence of strain F-32T (1479 21 bp). The sequence obtained was compared to reference 16S rRNA gene 22 sequences available in the GenBank, EMBL and DDBJ databases obtained 23 from the National Centre of Biotechnology Information database using the 24 BLAST search. Phylogenetic analysis was made using the software MEGA 25 version 3.0 (Kumar et al., 2004) after multiple data alignments by CLUSTALX 5 1 (Thompson et al., 1997). Distances and clustering were determined using the 2 neighbour-joining and maximum-parsimony methods. The stability of clusters 3 was ascertained by performing a bootstrap analysis (1000 replications). The 4 phylogenetic tree obtained by neighbour joining is shown in Figure 1. The 5 maximum-parsimony algorithm gave a similar result (data not shown). Our 6 results indicate conclusively that strain F32T belongs to the genus Alteromonas, 7 showing from 95.3% to 97.4% similarity with the other four species within the 8 genus. As expected, the next closest neighbours were the other members of the 9 Alteromonadaceae family, Glaciecola (Ivanova et al., 2004) and Aestuariibacter, 10 (Yi et al., 2004). The nucleotide-sequence characteristics of the family 11 Alteromonadaceae, 304 (A), 734 (A), 736 (T), 770 (T), 809 (A) (Ivanova et al., 12 2004) were present in strain F32T. 13 14 The fatty acids and quinones were analysed at the DSMZ (Deutsche Sammlung 15 von Mikroorganismen und Zellkulturen GmbH) in a culture of strain F-32T made 16 at 32oC in MY 7.5% w/v (see Table 2). The fatty-acid profile of strain F32T was 17 typical of Alteromonas species, with a predominance of 16:0, 16:1 ω7c, 18:1 18 ω7c, but it also contains large amounts of 16:0 N alcohol, 17:0 10 methyl, 18:0, 19 and an unusual unsaturated fatty acid (18:3 ω6c [6, 9, 12]). Unsaturated fatty 20 acids (PUFAs) are rare in mesophilic bacteria and have not been found so far in 21 any Alteromonas species. The predominant respiratory quinone was Q8 22 (ubiquinone 8, 96.5%; ubiquinone 7, 3.5%). 23 In conclusion, polyphasic analyses demonstrate that the new isolate 24 belongs to a consistent taxon and represents a novel species within the genus 25 Alteromonas, for which we propose the name Alteromonas hispanica. 6 1 Description of Alteromonas hispanica sp. nov. 2 3 Alteromonas hispanica (his pa’ ni ca: L. fem. adj. = Spanish) 4 5 The cells are straight rods 1-2 µm long and 0.75 µm wide, appearing either 6 singly or in pairs.
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