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Alteromonas Genovensis Sp. Nov., Isolated from a Marine Electroactive Biofilm and Emended Description of Alteromonas Macleodii Baumann Et Al

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Alteromonas Genovensis Sp. Nov., Isolated from a Marine Electroactive Biofilm and Emended Description of Alteromonas Macleodii Baumann Et Al International Journal of Systematic and Evolutionary Microbiology (2008), 58, 2589–2596 DOI 10.1099/ijs.0.65691-0 Alteromonas genovensis sp. nov., isolated from a marine electroactive biofilm and emended description of Alteromonas macleodii Baumann et al. 1972 (Approved Lists 1980) Ilse Vandecandelaere,1 Olivier Nercessian,2 Eveline Segaert,1 Wafa Achouak,2 Alfonso Mollica,3 Marco Faimali,3 Paul De Vos1 and Peter Vandamme1 Correspondence 1Laboratorium voor Microbiologie, Vakgroep Biochemie, Fysiologie en Microbiologie, Universiteit Ilse Vandecandelaere Gent, K. L. Ledeganckstraat 35, B-9000 Gent, Belgium [email protected] 2LEMiR, Laboratoire d’Ecologie Microbienne de la Rhizosphe`re, CNRS-CEA-Universite´ de la Me´diterrane´e, DEVM, Dpt Ecophysiologie Ve´ge´tale et de Microbiologie/DSV CEA Cadarache, 13108 Saint Paul Lez Durance, France 3Instituto di Scienze Marine – Consiglio Nazionale delle Ricerche (ISMAR-CNR), Via de Marini 6, 16149 Genoa, Italy Thirty-five isolates obtained from a marine electroactive biofilm grown on a stainless steel cathode (Genoa, Italy) were investigated by a polyphasic taxonomic approach. Whole-cell fatty acid methyl ester analysis indicated that the isolates belonged to the class Gammaproteobacteria and were closely related or belonging to the genus Alteromonas. Genomic fingerprinting using the BOX- PCR primer delineated five clusters of isolates with similar BOX-PCR fingerprints. This study demonstrated that isolates from four of the BOX-PCR clusters belonged to Alteromonas macleodii and that the 14 isolates representing BOX-PCR cluster 1 constituted a novel species, which shared 98.4 % 16S rRNA gene sequence similarity with its nearest phylogenetic neighbour, Alteromonas hispanica. Both phenotypic and genotypic analyses enabled this novel species, for which the name Alteromonas genovensis sp. nov. is proposed, to be differentiated from established species of the genus Alteromonas. The DNA G+C content of Alteromonas genovensis sp. nov. is 44.5 mol% and the type strain is LMG 24078T (5CCUG 55340T). The genus Alteromonas was created by Baumann et al. (Martı´nez-Checa et al., 2005), A. tagae (Chiu et al., 2007) (1972, 1984) to accommodate Gram-negative, strictly and A. simiduii (Chiu et al., 2007). aerobic, heterotrophic rods that are motile by a single The genus Alteromonas has gained increasing interest polar flagellum. Gauthier et al. (1995) restricted the genus because of potential industrial applications (Hayase et al., Alteromonas to the type species, Alteromonas macleodii, and 2003; Kodama et al., 1993; Martı´nez-Checa et al., 2005; transferred all the remaining species into the genus Raguenes et al., 2003, 1996; Shiozawa et al., 1993). Pseudoalteromonas. Since then, several marine bacteria have been classified as novel Alteromonas species and eight Van Trappen et al. (2004) emended the description of the further species have been described: Alteromonas macleodii genus Alteromonas by reporting the formation of prosthe- (Baumann et al., 1972), A. marina (Yoon et al., 2003), A. cae and buds in several species when grown for 3 or more stellipolaris (Van Trappen et al., 2004), A. litorea (Yoon et days at low temperatures. The presence of prosthecae and al., 2004), A. addita (Ivanova et al., 2005), A. hispanica buds enhances the bacterial surface : volume ratio, which facilitates substrate uptake in oligotrophic marine environ- ments (Van Gemerden & Kuenen, 1984). Marine prosthe- The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene cate bacteria also play a role in the corrosion of metals as T sequences of strains LMG 24078 , LMG 24079, LMG 24080, LMG they biologically catalyse the ennoblement of stainless steel 24081, LMG 24082 and LMG 24083 are AM885866, AM887686, surfaces (Baker et al., 2003). AM885868, AM885867, AM885870 and AM887685, respectively. DNA–DNA hybridization results and additional electron micrographs are The present study was part of an analysis of the microbial available with the online version of this paper. diversity of a marine electroactive biofilm grown on a Downloaded from www.microbiologyresearch.org by 65691 G 2008 IUMS Printed in Great Britain 2589 IP: 193.191.134.1 On: Thu, 02 Jun 2016 09:30:24 I. Vandecandelaere and others stainless steel cathode (EA-BIOFILMS-508866, NEST) Alteromonas species was investigated by repetitive DNA-PCR exposed to natural seawater at the ISMAR-CNR Marine (rep-PCR) fingerprinting using the BOX-A1R-primer (59- Station, located in the port of Genoa, Italy. Stainless steel CTACGGCAAGGCGACGCTGACG-39) (Versalovic et al., samples (25610 mm), cut from a UNS S 31254 plate 1994) as described by Rademaker & De Bruijn (1997) and (1 mm thick), were drilled, screwed and then treated Rademaker et al. (2000). Numerical analysis of the obtained with emery papers up to P1200. They were immersed in a DNA profiles using the BIONUMERICS 4.61 software (Applied tank of about 100 l natural seawater at ambient temper- Maths) revealed five clusters of isolates with similar BOX- ature. The seawater was continuously renewed at a rate of PCR profiles (at least 55.2 % intra-cluster profile similarity) about 1.5–2.0 l min21 with water pumped directly from (Fig. 1): cluster 1 (14 isolates), cluster 2 (9 isolates), cluster 3 the sea. (5 isolates), cluster 4 (3 isolates) and cluster 5 (4 isolates). The BOX-PCR profiles of these isolates also differed from The stainless steel electrode was cathodically polarized at those of the Alteromonas type strains. Each of the clusters 2200 mV Ag/AgCl (e.g. Faimali et al., 2008). Current comprised some isolates with virtually indistinguishable flowing from the ‘n’th polarized sample was calculated from profiles suggesting that they represent isolates of the same the ohmic drop, DV , measured across the resistor, R ,whose n n strain. However, each cluster also comprised isolates with value was chosen in such a way that a DV less than 10 mV n marked differences in their PCR fingerprints, indicating the was measured. During the tests, the cathodic current on all presence of multiple strains. polarized samples was regularly measured and recorded. The DNA G+C contents of representatives of each BOX- The current increased and stabilized at 0.5 A m22 in less PCR cluster were determined. DNA was degraded enzy- than 10 days and microscopic analysis (4006 magnifica- mically into nucleosides as described by Mesbah et al. tion using an Olympus BX41 epifluorescence microscope (1989). The nucleoside mixture obtained was then coupled with a UV filter block for DAPI) showed biofilm separated using a Waters Breeze HPLC system and formation on the cathode. The biofilm was removed from Xbridge Shield RP18 column thermostabilized at 37 uC. the stainless steel cathode by sonication (Branson 3200) The solvent was 0.02 M NH H PO (pH 4.0) with 1.5 % (90 s) in a sterile plastic tube containing 30 ml 0.85 % 4 2 4 acetonitrile. Non-methylated lambda phage (Sigma) and NaCl solution. Diluted cell suspensions (1021 to 1026) Escherichia coli LMG 2093 DNA were used as calibration were inoculated on marine agar (MA; Difco 2216) and reference and control, respectively. The DNA G+C incubated aerobically at 20 uC for several days. Pure contents of representatives of BOX-PCR clusters 1, 2, 3, 4 cultures were obtained and isolates were stored at and 5 were 44.6–45.4 mol%, which correlated with the 220 uCor280 uC using MicroBank vials. DNA G+C data reported for members of the genus All isolates were tentatively identified using whole-cell fatty Alteromonas (Gauthier et al., 1995) (see Supplementary acid methyl ester analysis as described by Mergaert et al. Table S1 in IJSEM Online). (2001). For 35 isolates, comparison of the fatty acid methyl Almost-complete 16S rRNA gene sequences (1339– ester profiles with a commercial database (MIS) indicated 1501 bp) were subsequently obtained for two representa- that they belonged to the class Gammaproteobacteria and that tives per BOX-PCR cluster using the universal primers pA they were closely related or belonged to the genus Altero- (59-AGAGTTTGATCCTGGCTCAG-39) and pH (59- monas. These data correlated with Alteromonas-like bacteria AAGGAGGTGATCCAGCCGCA-39; Edwards et al., 1989) constituting considerable fractions of attached marine as described previously (Mergaert et al., 2001). The FASTA microbial populations (Acinas et al., 1999; Dang & Lovell, program was used to find the most similar sequences in 2000). In addition, Alteromonas-like bacteria are also frequent public databases. Sequences were aligned using CLUSTAL_X producers of extracellular polymer substances, which is (Thompson et al., 1997) and edited using BIOEDIT (Hall, important in the context of biofilm formation (Branda et 1999) and FORCON (Raes & Van De Peer, 1999). A al., 2005; Flemming & Wingender, 2001). The dominant fatty neighbour-joining dendrogram was constructed (Saitou acids of the 35 isolates were C10 : 0 3-OH (2.2±0.8 %), C11 : 0 & Nei, 1987) using the TREECON software (Van De Peer & 3-OH (1.4±0.5 %), C (3.3±1.1 %), C 3-OH 12 : 0 12 : 0 De Wachter, 1994) (Fig. 2). (2.2±1.2 %), C14 : 0 (3.4±0.9 %), C15 : 1v8c (1.2±0.6 %), C16 : 0 (19.4±2.3 %), C17 : 0 (2.6±0.7 %), C17 : 1v8c (5.7± The similarity in 16S rRNA gene sequences among isolates 1.9 %), C18 : 0 (1.1±0.5 %), C18 : 1v7c (13.6±3.4 %), summed of the same BOX-PCR cluster was always ¢99.1 % (data feature 2 (which comprises any combination of C12 : 0 aldehyde, not shown). These results confirm that isolates with highly an unknown fatty acid of equivalent chain-length 10.928, iso- similar rep-PCR profiles are closely related (Rademaker & C16 : 1 IandC14 : 0 3-OH; 4.5±1.7 %) and summed feature 3 De Bruijn, 1997; Versalovic et al., 1994). (C v7c and/or iso-C 2-OH; 30.5±3.0 %); the remaining 16 : 1 15 : 0 Representatives of BOX-PCR clusters 2, 3, 4 and 5 exhibited fatty acids constituted minor fractions only (,1%).
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