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Phylogeny and Polyphasic Taxonomy of Caulobacter Species. Proposal of Maricaulis Gen International Journal of Systematic Bacteriology (1 999), 49, 1053-1 073 Printed in Great Britain Phylogeny and polyphasic taxonomy of Caulobacter species. Proposal of Maricaulis gen. nov. with Maricaulis maris (Poindexter) comb. nov. as the type species, and emended description of the genera Brevundirnonas and Caulobacter Wolf-Rainer Abraham,' Carsten StrOmpl,l Holger Meyer, Sabine Lindholst,l Edward R. B. Moore,' Ruprecht Christ,' Marc Vancanneyt,' B. J. Tindali,3 Antonio Bennasar,' John Smit4 and Michael Tesar' Author for correspondence: Wolf-Rainer Abraham. Tel: +49 531 6181 419. Fax: +49 531 6181 41 1. e-mail : [email protected] Gesellschaft fur The genus Caulobacter is composed of prosthecate bacteria often specialized Biotechnologische for oligotrophic environments. The taxonomy of Caulobacter has relied Forschung mbH, primarily upon morphological criteria: a strain that visually appeared to be a Mascheroder Weg 1, D- 38124 Braunschweig, member of the Caulobacter has generally been called one without Germany challenge. A polyphasic approach, comprising 165 rDNA sequencing, profiling Laboratorium voor restriction fragments of 165-235 rDNA interspacer regions, lipid analysis, Microbiologie, Universiteit immunological profiling and salt tolerance characterizations, was used Gent, Gent, Belgium to clarify the taxonomy of 76 strains of the genera Caulobacter, Deutsche Sammlung von Brevundimonas, Hyphomonas and Mycoplana. The described species of the Mikroorganismen und genus Caulobacter formed a paraphyletic group with Caulobacter henricii, Zellkulturen, Caulobacter fusiformis, Caulobacter vibrioides and Mycoplana segnis Braunschweig, Germany (Caulobacter segnis comb. nov.) belonging to Caulobacter sensu stricto. Dept of Microbiology and Caulobacter bacteroides (Brevundimonas bacteroides comb. nov.), C. henricii Immunology, University of subsp. aurantiacus (Brevundimonas aurantiaca comb. nov.), Caulobacter British Columbia, intermedius (Brevundimonas intermedia comb. nov.), Caulobacter Vancouver, British subvibrioides (Brevundimonas subvibrioides comb. nov.), C. subvibrioides Columbia, Canada subsp. albus (Brevundimonas alba comb. nov.), Caulobacter variabilis (Brevundimonas variabilis comb. nov.) and Mycoplana bullata belong to the genus Brevundimonas. The halophilic species Caulobacter maris and Caulobacter halobacteroides are different from these two genera and form the genus Maricaulis gen. nov. with Maricaulis maris as the type species. Caulobacter leidyia was observed to cluster with species of the genus Sphingomonas. Caulobacter crescentus is synonymous with C. vibrioides and C. halobacteroides is synonymous with Maricaulis maris as determined by these analyses and DNA-DNA hybridization. Biomarkers discerning these different genera were determined. The necessary recombinations have been proposed and a description of Maricaulis is presented. Keywords : Caulobacter, Brevundimonas, Maricaulis gen. nov., Mycoplana, Hyphomonas Abbreviations: DCI, desorption chemical ionization; FAB, fast atom bombardment; ISR, interspacer region; NFM, non-fat dry milk; SSCP, single-strand conformational polymorphism. The EMBL accession numbers for the 165 rDNA sequences reported in this paper are listed in Table 1. 00980 0 1999 IUMS 1053 W.-R. Abraham and others INTRODUCTION Strain CB5 IT was obtained independently from the Caulobacter All-Russian Collection of Microorganisms (VKM B- The genus is composed of dimorphic, 1496T)and from J. T. Staley (= DSM 9893T). prosthecate bacteria. In these prokaryotes, repro- duction results in the separation of two cells that are Fatty acids of Caulobacter spp. were determined by morphologically and behaviourally different from each Carter & Schmidt (1976) and polar lipids have been other. One sibling is non-motile, sessile by virtue of analysed by various groups (Minnikin et al., 1973; adhesive material and prosthecate, possessing at least Wilkinson, 1969; Wilkinson & Bell, 1971 ; Andreev et one elongated, cylindrical appendage (a prostheca) al., 1986; Batrakov et al., 1996, 1997). Using 5s rRNA that is an outgrowth of the cell envelope, including the sequences, Stackebrandt et al. (1 988) determined the outer membrane, the peptidoglycan layer and the cell phylogenetic position of Caulobacter crescentus within membrane (Staley, 1968). The other sibling is the a-subclass of the Proteobacteria; similar results flagellated, bearing one polar flagellum, by which it is were reported two years later by Nikitin et al. (1990). motile. The mode of reproduction of the dimorphic Anast & Smit (1988) were the first to determine prosthecate bacteria is unique as a regular feature of a differences between freshwater and marine caulo- prokaryotic reproductive cycle. It is regarded as a bacteria on a large set of strains. In a pioneering study, reflection of an ecological programme helping to Stahl et al. (1992) sequenced the 16s rRNA of several disperse the population at each generation, thereby Caulobacter isolates. Although sequences of type minimizing competition for resources. strains of Caulobacter species were not included in this In each species studied so far, the motile cell grows less study and a strain wrongly labelled as Caulobacter actively than its prosthecate sibling. Progress toward subvibrioides was included (Sly et al., 1997), this study reproduction is initiated in the swarmers only after this revealed, for the first time, that Caulobacter actually period of motility. It is consistent with this devel- forms two different lineages, one comprising the opmental and reproductive habit that these bacteria freshwater and brackish water Caulobacter spp. and exhibit the physiological properties of oligotrophs the other comprising the marine forms. Stahl et al. (Poindexter, 198 1a, b) and, most importantly, the (1992) also showed that Brevundirnonas dirninuta tolerance of prolonged nutrient scarcity. Once isolated, (Segers et al., 1994) clusters within the group of individual strains may tolerate much higher nutrient freshwater Caulobacter spp. The 16s rDNA sequences concentrations than are useful for their enrichment of Mycoplana segnis and Mycoplana bullata (Yanagi & and isolation. All caulobacteria are oxybiotic and Yamasato, 1993) also fall in the freshwater grow in well-aerated cultures. CaulobacterlBrevundirPzonascluster and thus compli- cate the taxonomy further. Caulobacteria are ubiquitous in water. As typical aquatic bacteria, they may be second only to pseudo- As caulobacteria are ubiquitous in water samples and monads in the breadth of their distribution and are believed to play an important role in the carbon numbers (Lapteva, 1987). These two bacterial groups cycling within their habitats, the intent of the present together are presumed to be responsible for con- study was to evaluate the diversity of freshwater and siderable mineralization of dissolved organic material marine caulobacters using lipid analysis, immuno- in aquatic environments, whereby the oligotrophic logical profiling and 16s rRNA gene sequences to caulobacters are especially important when nutrient compare these results with physiological data. Because concentrations and ambient temperatures are low previous studies (Stahl et al., 1992) revealed a close (Staley et al., 1987). Practically any type of seawater ph ylogenetic distance be tween Caulobac ter , Hypho- contains Caulobacter (Jannasch & Jones, 1960; Anast rnonas jannaschiana, Mycoplana bullata, Mycoplana & Smit, 1988) and, further, MacRae & Smit (1991) segnis and B. dirninuta, strains of these genera were reported the ready detection of Caulobacter in highly also included in this study. aerobic activated sewage sludge. The first isolation of a Caulobacter sp. was reported by METHODS Loeffler (1 890). He noticed the unusually low nutrient requirements of the strain. He could not assign the Strains and culture conditions. The strains in this study were strain to a known taxon and named this ‘hochst obtained from the American Type Culture Collection merkwurdigen Organismus ’ ‘ Vibrio (?) spermato- (ATCC), the Deutsche Sammlung von Mikroorganismen .zoides’. Later, Henrici & Johnson (1935) described the und Zellkulturen (DSMZ ; DSM strains), the Laboratorium genus Caulobacter with Caulobacter vibrioides as the voor Microbiologie, Universiteit Gent, Belgium (LMG strains), the All-Russian Collection of Microorganisms type species. Then, Poindexter (1964) enlarged the (VKM), from Ingo Fritz at the GBF (Brevundimonas sp. imonotypic genus considerably by describing nine B0.07 and BO.10) and from the Dept of Microbiology and species and two subspecies, and later added Caulo- Immunology at the University of British Columbia (CB, bacter variabilis (Poindexter, 1989). FWC and MCS strains). Table 1 shows the origin of the Henrici & Johnson (1935) did not isolate Caulobacter isolates. vibrioides and therefore a type strain was not named. All strains were grown in medium PYEM with the exception Poindexter (1964) proposed strain CB5 1 as the neotype of Caulobacter maris ATCC 1526gT, Caulobacter halo- strain of C. vibrioides (Poindexter & Lewis, 1966). bacteroides ATCC 15269T, Hyphomonas spp. and all Caulo- 1054 lnterna tional Journal of Systematic Bacteriology 49 Phylogeny of caulobacteria Table 7. List of strains used in this study including their serum reactions and the accession numbers of the newly determined 165 rRNA gene sequences Strain Source Positive Accession reaction no. with serum: Brevundimonas diminuta LMG 2089T Freshwater SMT2 A5227778 Brevundimonas diminuta LMG 2337 Blood,
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