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1 Max-Planck-Institute for Molecular Genetics, Department of Vertebrate Genomics, Ihnestraße 73, 14195 Berlin, Germany
2 GBF – National Research Center for Biotechnology, Division of Microbiology, Mascheroder Weg 1, D-38124 Braunschweig, Germany
3 Institute of Microbiology, Russian Academy of Sciences, Prospect 60-Letiya Octyabrya 7, korp 2, Moscow 117811, Russia
Correspondence
Wolf-Rainer Abraham
wab{at}gbf.de
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8c, 11-Me-C18 : 15t). The results of DNA–DNA hybridization and physiological and biochemical tests allowed genotypic and phenotypic differentiation of the strains from all recognized Brevundimonas species. The strains therefore represent a novel species, for which the name Brevundimonas mediterranea sp. nov. is proposed, with the type strain V4.BO.10T (=LMG 21911T=CIP 107934T).
Published online ahead of print on 5 November 2004 as DOI 10.1099/ijs.0.02852-0.
The GenBank/EMBL/DDBJ accession numbers for the 16S rRNA gene sequences of strains V4.BO.07, V4.BO.10T, LMG 9567t1, LMG 11070, LMG 9564, V4.BO.05, V4.BO.22, V4.BO.18, V4.BE.56, V4.BO.27, V4.BE.49 and V4.BP.05 are AJ227800, AJ227801, AJ244647–AJ244649 and AJ244704–AJ244710.
Strain details, transmission electron micrographs, protein profiles and RAPD profiles are available as supplementary material in IJSEM Online.
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into a new genus Brevundimonas with Brevundimonas diminuta as the type species of the genus. In 1999 several species were transferred from the genus Caulobacter to Brevundimonas and the description of the genus Brevundimonas was emended (Abraham et al., 1999). Brevundimonas species are characterized and differentiated from Caulobacter species by the presence of certain glyco- and polar lipids, outer-membrane proteins and an increased salt tolerance, but members of the genus show diverse cell morphologies and substrate specificities. Although some marine Brevundimonas strains have been described (Stahl et al., 1992; Yokoyama et al., 1996; Abraham et al., 2002), no marine Brevundimonas species has been named to date. Here we describe six strains isolated from marine water samples, which we propose are representatives of a novel species, Brevundimonas mediterranea sp. nov.
Sampling
Marine water samples were taken aboard the ship Thetys II (Institute National des Sciences de l’Univers INSU - CNRS/France) at two stations located in the north-western basin of the Mediterranean Sea on a transect between Nice and Corsica. Stations S1 [5·5 nautical miles (about 10 km) from the coast, nautical coordinates 43° 37' 48'' N 7° 26' 06'' E] and station S2 [28 nautical miles (about 52 km) from the coast, nautical coordinates 43° 25' 00'' N 7° 52' 00'' E] were sampled in early April 1995. Samples were collected with 12 litre Niskin bottles during the early afternoon and were stored in HCl-washed polycarbonate tanks until return to the institute. Plating was performed in triplicate either directly on Difco marine broth (MB) agar (representing the total biocoenosis) or using either the filtrate (representing the free-living biocoenosis) or the resuspended residue (representing the particle-bound biocoenosis) from 1 µm Nucleopore-filtered marine water samples (Fritz, 2000). After 2 weeks of dark incubation at ambient temperature, plate counts were performed and bacterial colonies were isolated.
Isolation and morphological diagnosis
Plates occasionally showed an abundance of a distinct type of bacteria with unique colony morphology. Bacterial colonies were cream-white in colour with a central brownish spot and had a slimy consistency; depending on age, colonies measured between 2 and 8 mm in diameter and contributed to more than 50 % of all colony-forming units in all triplicates of some investigated water samples (Fritz, 2000). Colony-forming units with this distinct, highly characteristic morphology were observed in water samples from both stations, from both free-living and particle-bound biocoenosis and from various depths. Six strains (V4.BE.49, V4.BE.56, V4.BO.10T, V4.BO.18, V4.BO.22 and V4.BO.27) with the described colony morphology originating from water samples from both stations and various depths were purified to macroscopic and microscopic homogeneity (see Supplementary Table A for details of their properties, available in IJSEM Online). Microscopically, the cells consisted of flexible, slightly bent long rods with a length of 1·5–4 µm and a diameter of 0·5–1 µm (Supplementary Fig. A). These six strains are hereafter referred to as operational taxonomic unit (OTU) H (Fritz, 2000).
16S rRNA gene sequencing
16S rRNA gene sequence analysis, conducted as described by Abraham et al. (1999), showed that the six OTU H strains were very similar, with sequence similarities exceeding 99·8 %, and that they formed a distinct lineage within the genus Brevundimonas (Fig. 1). The closest recognized relatives of strain V4.BO.10T were the unpigmented prosthecate strain Brevundimonas intermedia ATCC 15262T and the red-pigmented Brevundimonas vesicularis LMG 2350T, with respective sequence similarities of 99·4 and 99·2 %. Slightly more distantly related were Brevundimonas aurantiaca DSM 4731T (98·9 %) and the recently discovered Brevundimonas nasdae GTC 1043T (99·0 %) (Li et al., 2004). To provide further detail of the taxonomic relations within the genus Brevundimonas, the 16S rRNA gene sequences of three hitherto phylogenetically unaffiliated Brevundimonas strains, LMG 9564, LMG 9567t1 and LMG 11070 (Segers et al., 1994), were determined. Among these strains, the unpigmented Brevundimonas sp. LMG 11070 appeared to be a close relative of OTU H, whereas the red-pigmented strains LMG 9564 and LMG 9567t1 showed close phylogenetic relationships to B. aurantiaca and B. vesicularis, respectively. In addition, strain LMG 19834, characterized by Mergaert et al. (2001), showed a close relationship to OTU H. Thus OTU H, LMG 11070 and LMG 19834 formed a monophyletic cluster within the genus Brevundimonas. This topology was supported by maximum parsimony and maximum likelihood and in 93 % of the neighbour-joining bootstrap calculations. Within this cluster, strain V4.BO.18 formed a subcluster together with strains LMG 11070 and LMG 19834, due to a 3 nt exchange (i.e. 0·2 %) common to these three strains in the 1416 bp sequence investigated.
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, UPGMA clustering of binary presence/absence patterns based on matched gel bands reliably distinguished OTU H strains from their closest recognized relatives using all investigated fingerprint techniques.
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; Supplementary Fig. B). The profiles of V4.BO.18 and LMG 11070 differed slightly from the other protein profiles of OTU H in the region between 75 and 100 kDa. By contrast, the protein profiles from B. aurantiaca DSM 4731T, B. vesicularis LMG 2350T and B. intermedia ATCC 15262T were more heterogeneous and appeared clearly different from those of the OTU H strains.
As shown by Fritz (2000), all six OTU H strains possessed identical low-molecular-mass RNA (LMW-RNA) profiles, which differed at least in the size of one distinct band to all recognized Brevundimonas species. Höfle (1998) indicated that identical LMW-RNA profiles point to a degree of relatedness at the species level. Indeed, the type strains of B. vesicularis, B. intermedia and B. aurantiaca shared an identical LMW-RNA profile [Fig. 2b; see scanned gel in Fritz (2000), p. 126], but were not related at the species level, as shown by DNA–DNA hybridization data (Table 1) and various other approaches (Abraham et al., 1999; Li et al., 2004). This demonstrates that LMW-RNA profiles can be used to differentiate Brevundimonas strains above species but below the genus level. Consequently, LMW-RNA profile analysis supports the view of an affiliation of OTU H within a distinct Brevundimonas species (Fritz, 2000). The LMW-RNA profile of strain LMG 11070 differed from that of the OTU H strains.
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. The monophyly of OTU H was supported in 95·8 % of 1000 bootstrap analyses (Fig. 2c; Supplementary Fig. C). However, the RAPD fingerprints of OTU H were similar but not identical. Instead, OTU H could be differentiated into three RAPD fingerprint types. Type 1 consisted of three strains isolated from the oligotrophic station, strains V4.BO.10T, V4.BO.22 and V4.BO.27, but not strain V4.BO.18. Type 2 consisted of both strains from the eutrophic station, V4.BE.49 and V4.BE.56. V4.BO.18 had a unique RAPD fingerprint type. Thus OTU H consisted of three clonal lineages. Strain LMG 11070 could not be affiliated with any of the three fingerprint types.
G+C content, genome size and DNA–DNA hybridization
The DNA G+C contents of OTU H ranged between 67·1 and 67·5 mol% (Supplementary Table A). This is slightly higher than the G+C contents measured for B. intermedia ATCC 15262T (66·1 mol%), B. vesicularis LMG 2350T (66·2 mol%) and B. aurantiaca DSM 4731T (65·6 mol%). For strain LMG 11070, Segers et al. (1994) determined a G+C content of 67·0 mol%. The genome size of strain V4.BO.10T, as determined by the method of Gillis et al. (1970), was 2·4x109 Da. Similar genome sizes were determined for B. intermedia ATCC 15262T (2·2x109 Da), B. vesicularis LMG 2350T (2·3x109 Da) and B. aurantiaca DSM 4731T (2·4x109 Da). DNA–DNA hybridization data are shown in Table 1. For strain V4.BO.10T, no DNA relatedness exceeding 33 % was measured, which is well below the generally accepted value of 70 % for intraspecies strains (Wayne et al., 1987).
Lipid analysis
For OTU H, fatty acids have been reported to be similar to those of B. intermedia and the polar lipids were phosphatidyl diacylglycerol (720, 734, 746, 748, 760, 762, 774 and 788 Da), sulfoquinovosyl diacylglycerol (820 and 834 Da) and phosphatidyl glucopyranosyl diacylglycerol (PGL; 1411, 1413, 1425, 1427, 1439, 1453 Da) (Abraham et al., 1997). The cellular fatty acids of strain V4.BO.10T comprised C14 : 0 (0·6 %), C15 : 0 (5·4 %), 3-OH-C12 : 0 (2·0 %), C16 : 0 (16·1 %), C17 : 0 (6·1 %), C18 : 0 (0·9 %), C16 : 1 (8·4 %), C17 : 16c (7·8 %), C17 : 18c (9·9 %), C18 : 1 (36·7 %), 11-Me-C18 : 15t (4·2 %) and ECL 17.897 (1·6 %), similar to those of Brevundimonas sp. LMG 11070, and with larger amounts of C15 : 0 and C17 : 18c and smaller amounts of C18 : 1 compared with B. intermedia and B. vesicularis (Abraham et al., 1997). OTU H differed from the recently described B. nasdae (Li et al., 2004) by the presence of considerable amounts of C15 : 0, larger amounts of summed feature 4 fatty acids, the presence of fatty acid ECL 17.897, larger amounts of 11-Me-C18 : 15t and summed feature 7 fatty acids and the lack of C19 : 0 cyclo 8c.
Substrate utilization
Good growth of the OTU H strains was obtained at 30 °C and NaCl concentrations between 1 and 3 % (w/v). Further details are given in the species description. Strain LMG 11070 did not tolerate NaCl concentrations above 1 % (w/v). No nitrogen fixation was detected, as tested by growth experiments in Burk's nitrogen-free medium (Smibert & Krieg, 1981), which was adjusted to an NaCl concentration of 3 % (w/v).
The results from substrate specificity tests, as determined by API galleries (bioMérieux) and from Biolog substrate utilization tests, are given in detail in the species description. Criteria for differentiation on the basis of substrate utilization patterns between the OTU H strains as well as closely related Brevundimonas species and isolates are given in Table 2.
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and the species description). The strains could be differentiated from B. vesicularis by the presence of 
-glucosidase activity and from B. intermedia by the lack of chymotrypsin and -galactosidase activity.
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). Further investigations are required to clarify the taxonomic status of this strain. With regard to strain LMG 19834, Mergaert et al. (2001) reported its inability to reduce nitrate to N2 and that, in contrast to the OTU H strains, LMG 19834 formed stalks. As we did not investigate this strain in detail, we cannot determine whether strain LMG 19834 and OTU H are related at the species level.
Although generally regarded as non-marine bacteria, reports on Brevundimonas strains isolated from marine habitats have accumulated (Stahl et al., 1992; Yokoyama et al., 1996; Abraham et al., 2002). Two marine Brevundimonas sp. strains, MCS 17 and MCS 24 (Stahl et al., 1992; Abraham et al., 2002), for which 16S rRNA gene sequence data have been published, showed relatively distant phylogenetic relationships (96·1–96·7 % similarity) with OTU H (Abraham et al., 1999) (Fig. 2). During sampling in the Mediterranean Sea, from a total of 227 isolated strains, three further Brevundimonas strains were isolated (Fritz, 2000). The red-pigmented strains V4.BO.05 and V4.BO.07 (designated OTU H' in Fritz, 2000) were closely related to B. vesicularis, whereas the brown-pigmented strain V4.BP.05 (designated OTU H* in Fritz, 2000) was similar but not identical to Brevundimonas subvibrioides. However, as revealed by plate counts, no abundance of colony-forming units with similar morphologies to these strains was detected in any of the water samples investigated by Fritz (2000). Analyses of a clone library from excised DGGE bands derived from RNA extracts from the Mediterranean water samples revealed the presence of a clone with a partial 16S rRNA gene sequence similar to Brevundimonas alba (I. Fritz, unpublished, accession number AJ508416), suggesting an abundance of further Brevundimonas species in marine water samples.
Based on the data presented, we propose that the six OTU H strains cannot be affiliated within any recognized Brevundimonas species. The closest recognized relative of the OTU H strains is B. intermedia, which differs on the basis of morphology, genome size, presence of chymotrypsin and -galactosidase activity and absence of PGLs of 1411 Da (Abraham et al., 1997). The OTU H strains differ from B. vesicularis by having thicker cells, the presence of -glucosidase, smaller amounts of C15 : 0, C16 : 1 and C17 : 18, but larger amounts of C18 : 1, the presence of phosphatidylglycerols of 720, 734, 746, 760 and 788 Da and the presence of PGL of 1411 Da. OTU H can be distinguished from the recently described B. nasdae GTC 1043T (Li et al., 2004) by the presence of C15 : 0 and ECL 17.897, larger amounts of 11-Me-C18 : 15t and the lack of C19 : 0 cyclo 8c in the cellular fatty acids, a higher G+C content, the ability to grow at NaCl concentrations of 4 % (w/v), the ability to utilize fructose but not succinate and n-capric acid as well as the presence of urease activity in some strains. Furthermore, the OTU H strains can be differentiated from their closest recognized relatives by DNA–DNA hybridization, 16S rRNA gene sequencing, LMW-RNA profile analysis, protein fingerprints and substrate utilization patterns. Therefore, we propose to include the six OTU H strains within a novel species, Brevundimonas mediterranea sp. nov., with V4.BO.10T as the type strain.
Description of Brevundimonas mediterranea sp. nov.
Brevundimonas mediterranea (me.di.ter.ra'ne.a. N.L. fem. adj. mediterranea of the Mediterranean Sea).
The description is as that of the genus with the following additions. Colonies measure 2–5 mm in diameter on MB agar, have a soft and slimy consistency with a glistening surface and smooth margin, a slightly concave shape and are cream-white coloured with a characteristic slightly brownish spot in the centre. Pigmentation is not present. Flexible, non-stalked, occasionally bent rods with a length of 1·5–4 µm and a diameter of 0·5–1·0 µm. Some strains but not the type strain may possess a branching cell morphology.
Alkaline and acid phosphatase, esterase (C4), esterase lipase (C8), - and weak 
-glucosidase, leucine arylamidase, valine arylamidase and trypsin activities are always positive. Activities for the following enzymes are not detected: chymotrypsin, cystine arylamidase, -fucosidase, -galactosidase, -galactosidase, -glucuronidase, lipase (C14), -mannosidase and N-acetylglucosaminidase. Urease activity is present in some strains but not the type strain. Gelatin is not liquefied. Aesculin is hydrolysed. As determined by API galleries, the following substrates are utilized by all strains: amygdalin, arbutin, cellobiose, D-fructose, gentiobiose, -D-glucose, -hydroxybutyric acid, maltose, salicin and starch. The following substrates are used as sole carbon and energy sources by some strains including the type strain: L-arabinose, fumarate, L-glutamate, DL-lactate, L(–)-malate, maltotriose, L-proline, propionate and turanose. The following substrates were utilized by some strains but not by the type strain: adipate, L-alanine, rhamnose and L-serine. The following substrates are not utilized: D(+)-malate, malonate, maltitol, mannitol, D-mannose, melezitose, melibiose, methyl -D-glucopyranoside, methyl -galactopyranoside, methyl -galactopyranoside, methyl -glucopyranoside, methyl -D-mannoside, methyl -xyloside, mucate, palatinose, phenylacetate, 3-phenylpropionate, protocatechuate, putrescine, (–)-quinate, D-raffinose, D(–)-ribose, D-saccharate, D-sorbitol, L-sorbose, D-tagatose, D(–)-tartrate, L(+)-tartrate, meso-tartrate, trehalose, tricarballylate, trigonelline, tryptamine, tyrosine, L-xylitol, xylitol, D-xylose and L-xylose.
As measured by Biolog tests, Tween 40 and -cyclodextrin serve as electron donors for the artificial electron acceptor tetrazolium violet and thus may be metabolized by all strains. Some strains including the type strain use acetic acid, alaninamide, 
-aminobutyric acid, 2-aminoethanol, L-asparagine, 2,3-butanediol, dextrin, D-galactonic acid lactone, glycyl L-aspartic acid, glycyl L-glutamic acid, hydroxy-L-proline, methylpyruvate, monomethyl succinate, L-ornithine, L-pyroglutamic acid, sebacic acid, L-threonine and Tween 80 as electron donors. L-Alanyl glycine is utilized by some strains but not by the type strain. None of the following are used as electron donors by any strain: N-acetyl-D-galactosamine, bromosuccinic acid, DL-carnitine, formic acid, D-glucosaminic acid, glucose 1-phosphate, glucose 6-phosphate, glucuronamide, DL--glycerol phosphate, -hydroxybutyric acid, -hydroxybutyric acid, p-hydroxyphenylacetic acid, inosine, -ketobutyric acid, -ketoglutaric acid, -ketovaleric acid, L-leucine, phenylethylamine, L-phenylalanine, D-psicose, D-serine, succinamic acid, succinic acid, sucrose, thymidine, uridine and urocanic acid.
NaCl is not strictly required but promotes growth at optimal concentrations. The optimum NaCl concentration for growth is 1 % (w/v), with good growth at 0–3 % and no growth at 6 % or above. Optimal growth temperature is 30 °C. The species grows between 15 and 37 °C, but not above 42 °C. Some strains including the type strain show weak growth at 7 °C. Nitrogen is not fixed. Neither nitrate nor nitrite is utilized as a terminal electron acceptor with the exception of strain V4.BO.18, which is capable of reducing nitrate to nitrite but not to nitrogen. Polar lipids are 18 : 1/14 : 0-, 18 : 1/15 : 0-, 18 : 1/16 : 1-, 18 : 1/16 : 0-, 18 : 1/17 : 1-, 18 : 1/18 : 1-, 19 : 1/16 : 0- and 19 : 1/18 : 1-PG, 18 : 1/17 : 0-SQDG and PGLs of 1411, 1413, 1425, 1427, 1439 and 1453 Da. The main fatty acids of the cellular hydrolysate are C18 : 1, C16 : 0, C16 : 1, C15 : 0, C17 : 18c, C17 : 16c, C17 : 0 and 11-Me-C18 : 15t; the main hydroxy-fatty acid is 3-OH-C12 : 0. The G+C content is between 67·1 and 67·5 mol%. Main ubiquinone is Q-10 (Abraham et al., 1999). DNA–DNA relatedness between strain V4.BO.10T and B. intermedia ATCC 15262T, B. vesicularis LMG 2350T and B. aurantiaca DSM 4731T is 27, 33 and 33 %, respectively.
Strain V4.BO.10T (=LMG 21911T=CIP 107934T) is the type strain. The strains were isolated from water samples from the western Mediterranean Sea near Nice.
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ACKNOWLEDGEMENTS |
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