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1 Institute of Microbiology, Russian Academy of Sciences, Prospekt 60-letiya Oktyabrya 7/2, Moscow 117811, Russia
2 UMR 6539, Centre National de la Recherche Scientifique and Université de Bretagne Occidentale, Institut Universitaire Européen de la Mer, 29280 Plouzané, France
3 DSMZ – German Collection of Microorganisms and Cell Cultures, Mascheroder Weg 1b, 38124 Braunschweig, Germany
Correspondence
M. L. Miroshnichenko
alfamirr{at}mail.ru
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ABSTRACT |
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The GenBank accession number for the 16S rDNA sequence of Caminibacter profundus strain CRT is AJ535664.
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MAIN TEXT |
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TOPABSTRACTMAIN TEXTREFERENCES |
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). The family Campylobacteraceae contains the genera Campylobacter, Arcobacter, Sulfurospirillum and Thiovulum, whereas the family ‘Helicobacteraceae’ is formed by the genera Helicobacter and Wolinella. These bacteria are mesophiles adapted to environments that are low in oxygen. Most of them are oxidase-positive microaerophiles, but numerous members also grow in the absence of oxygen (Vandamme et al., 1991). Among them, Sulfurospirillum halorespirans and Sulfurospirillum multivorans have been described recently as obligate anaerobes (Luijten et al., 2003). All the above-mentioned genera, except for Thiovulum and Sulfurospirillum, which thrive in aquatic habitats, have been found associated with animals.
Assessment of microbial diversity using molecular phylogenetic approaches has revealed that members of the ‘Epsilonproteobacteria’ dominate various deep-sea hydrothermal habitats such as microbial mats of Loihi Seamount (Moyer et al., 1995), surfaces of invertebrates (Haddad et al., 1995; Polz & Cavanaugh, 1995; Cary et al., 1997) and sulfides from the Mid-Atlantic Ridge (Reysenbach et al., 2000; Corre et al., 2001) and southern East Pacific Rise (Longnecker & Reysenbach, 2001). Recently, thermophilic representatives of the ‘Epsilonproteobacteria’ have been isolated from tube fragments of Alvinella pompejana, an annelid polychaete endemic to chimney walls of the East Pacific Rise hydrothermal vents. Both Nautilia lithotrophica and Caminibacter hydrogeniphilus are strictly anaerobic hydrogen-oxidizers able to grow chemolithoautotrophically with sulfur as electron acceptor (Miroshnichenko et al., 2002; Alain et al., 2002). Other organisms that are phylogenetically closely related and phenotypically similar to these species have been partially characterized by Campbell et al. (2001). All these thermophilic isolates, along with a number of environmental sequences retrieved from hydrothermal systems, form a deep monophyletic unit within the ‘Epsilonproteobacteria’. Very recently, many novel phylogenetically diverse representatives of the ‘Epsilonproteobacteria’ have been isolated from the hydrothermal fields of the Okinawa Trough and Central Indian Ridge and partially described (Takai et al., 2003). Here, a second species in the genus Caminibacter, Caminibacter profundus sp. nov., isolated from a hydrothermal vent of the Mid-Atlantic Ridge, is described.
Strain CRT was isolated from material collected using a vent cap at the Rainbow hydrothermal vent field (36°16'N; 33°54'W; 2400 m depth) on the Mid-Atlantic Ridge during the Iris cruise in May 2001. An in situ growth chamber or vent cap (Reysenbach et al., 2000), designed to concentrate the micro-organisms discharged by hydrothermal emissions, was deployed using the hydraulic arm of the remotely operated vehicle Victor. After incubation in situ for 2 days, the vent cap was closed by the hydraulic arm of the remotely operated vehicle before transportation to the surface. Once on board, the vent cap content was immediately transferred to 50 ml glass vials and flooded with a sterile solution of 3 % (w/v) sea salts (Sigma). The vials were then closed tightly with butyl rubber stoppers (Bellco), pressurized with N2 (100 kPa), reduced with sodium sulfide and stored at 4 °C until further processing in the laboratory.
For enrichment, the following basal medium (BM) was used (g l-1, unless otherwise stated): NH4Cl, 0·33; KCl, 0·33; KH2PO4, 0·33; CaCl2.2H2O, 0·33; MgCl2.6H2O, 0·33; NaCl, 25·0; yeast extract, 0·1; trace elements (Balch et al., 1979), 10 ml l-1; vitamins (Wolin et al., 1963), 10 ml l-1. The medium was prepared anaerobically and dispensed into Bellco tubes; the headspace (25 ml) was filled with H2/CO2, (80 : 20, 200 kPa). No reducing agents were added to the medium. Elemental sulfur was added to a final concentration of 10 g l-1. The pH of the medium was adjusted with 2·5 M H2SO4 to 6·8–7·0. When substrates other than molecular hydrogen were tested, the headspace was filled with N2/CO2 (8 : 2, v/v, atmospheric pressure). A pure culture was obtained on the same basal medium without yeast extract using a serial tenfold dilution technique. Morphology of the novel isolate was examined using an Olympus BX-60 microscope. The ultrastructure of whole cells and thin sections was studied as described elsewhere (Bonch-Osmolovskaya et al., 1990). For physiological studies, the isolate was grown on BM medium containing MOPS (10 mM) as a buffer. The pH of the medium was adjusted to 7·0 with 5 M NaOH before autoclaving. Potential growth substrates and electron acceptors were added at concentrations of 0·3 and 0·2 % (w/v), respectively. The ability of the isolate to grow microaerobically and/or aerobically was tested on BM medium, with oxygen added to the H2/CO2 mixture (80 : 20, v/v, 200 kPa); the final concentration of oxygen varied from 0·25 to 20 %. Carbon source utilization was determined using substrates at a concentration of 0·05 %; in this case, the headspace was filled with 100 % H2 (atmospheric pressure). Inoculated tubes were incubated at 55 °C. The cell density was determined by direct cell counting using a light microscope. Gaseous and liquid fermentation products, as well as the products of nitrate reduction, were detected as described previously (Miroshnichenko et al., 1994, 2003). Hydrogen sulfide was measured by a colorimetric method (Trüper & Schlegel, 1964). The sensitivity of strain CRT to rifampicin, chloramphenicol, vancomycin, penicillin, streptomycin and tetracycline (Sigma) was tested at a concentration of 100 µg ml-1. Determination of the DNA G+C content was performed as described elsewhere (Miroshnichenko et al., 2003). DNA extraction, PCR amplification of the 16S rRNA gene and determination of the sequence followed described methods (Rainey et al., 1996). The 16S rRNA sequences were aligned with published sequences of the DSMZ database using the ae2 editor (Maidak et al., 1999) and sequences retrieved from EMBL. Evolutionary distances were calculated by the method of Jukes & Cantor (1969). Distance analysis dendrograms were reconstructed by the neighbour-joining algorithm. Bootstrap analysis was used to evaluate the tree topology by performing 500 resamplings (Felsenstein, 1988).
Enrichment was performed in Bellco tubes filled with 5 ml BM medium. A H2/CO2 mixture (80 : 20, 200 kPa) served as the energy and carbon source, and elemental sulfur was the electron acceptor. After inoculation of BM medium with 0·5 ml material recovered from the vent cap content and inner surfaces and incubation of the tubes for 3 days at 55 °C without shaking, growth of non-motile rods was observed, accompanied by the formation of hydrogen sulfide. Transfer of the enrichment culture into BM medium without yeast extract did not affect its growth. A pure culture, CRT, was isolated by serial dilutions in liquid mineral medium. Purity of the culture was checked by the absence of growth in a non-selective glucose- and peptone-containing medium (each at 3 g l-1).
Cells of strain CRT were rod-shaped (approximately 1·2–1·5x0·5 µm) and motile in the exponential phase of growth. One polar flagellum was present on negatively stained whole-cell preparations (Fig. 1a). Formation of spores was not observed. Thin sectioning revealed the Gram-negative structure of the cell wall (Fig. 1b).
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Comparison of the 16S rRNA gene sequence (1414 bases) with those of members of the domain Bacteria indicated that strain CRT belonged to the class ‘Epsilonproteobacteria’ and was moderately related to C. hydrogeniphilus (94·9 % similarity) and N. lithotrophica (91·2 % similarity), both of which were isolated from 13°N on the East Pacific Rise. Strain CRT showed higher sequence similarity (92·3–96·1 %) to a group of clone sequences retrieved from material from deep-sea hydrothermal vents on the Mid-Atlantic Ridge (VC2.1Bac7, VC2.1Bac17, VC2.1Bac8, VC2.1Bac30; Reysenbach et al., 2000). Slightly lower similarities (91·4–93·7 %) were found to clone sequences retrieved from South-East Pacific vents (S17sBac14, S17sBac3, S17sBac5; Longnecker & Reysenbach, 2001) and to isolate AM1115 (Alain et al., 2002).
The phylogenetic relatedness of strain CRT to C. hydrogeniphilus is consistent with shared physiological characteristics and the DNA G+C content (Table 1). Both strains are moderately thermophilic chemolithoautotrophs, growing with hydrogen as electron donor and elemental sulfur or nitrate as electron acceptors. However, C. hydrogeniphilus has been described as a strictly anaerobic micro-organism, whereas strain CRT is able to grow anaerobically and microaerobically at an oxygen concentration of up to 2 %. The isolate has a narrow pH growth optimum of 6·9–7·1, whereas C. hydrogeniphilus grows optimally at pH 5·5–6·5. In contrast to C. hydrogeniphilus, which is capable of poor heterotrophic growth on complex organic substrates, strain CRT is a strictly lithotrophic micro-organism. Thus, on the basis of phylogenetic, morphological and physiological features, it is proposed that CRT (=DSM 15016T=JCM 11957T) is the type strain of a novel species of Caminibacter, for which the name Caminibacter profundus sp. nov. is proposed.
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) is represented by a single tentative order, ‘Campylobacterales’. The order presently contains the family Campylobacteraceae (Vandamme & De Ley, 1991) and the as-yet tentative family ‘Helicobacteraceae’ (Garrity & Holt, 2001). Levels of 16S rRNA gene sequence similarity between the lineage encompassing Nautilia and Caminibacter and the ‘Campylobacterales’ are about 83 % (Fig. 2). Phenotypic and genomic features also clearly distinguish the two phylogenetic lineages (Table 1
). It is therefore proposed that members of the genera Nautilia and Caminibacter form a new order, Nautiliales ord. nov., represented by the single family Nautiliaceae fam. nov.
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Order of the ‘Epsilonproteobacteria’ separate and distinct from the ‘Campylobacterales’. Segregation of these organisms into a new order is justified by (i) their distinct phylogenetic position and (ii) their thermophilic way of life. Marine thermophilic rod-shaped bacteria, mean cell size of 0·5x1·3 µm, non-spore-forming. Gram-negative. Obligately anaerobic or microaerobic. For anaerobic growth, sulfur or nitrate are used as electron acceptors. Chemolithoautotrophs; mixotrophy occurs. Positive for H2 oxidation. DNA G+C content of 29–35 mol%. Type genus: Nautilia Miroshnichenko et al. 2002.
Description of Nautiliaceae fam. nov. Miroshnichenko et al.
Nautiliaceae (Nau.ti'li.a.ce.ae. N.L. fem. n. Nautilia the type genus of the family; N.L. -aceae ending denoting a family; N.L. fem. pl. n. Nautiliaceae the family of Nautilia).
Description is the same as that for the order. Type genus: Nautilia Miroshnichenko et al. 2002.
Description of Caminibacter profundus sp. nov.
Caminibacter profundus (pro.fun'dus. L. masc. adj. profundus of the depths of the ocean).
Cells are motile, rod-shaped (1·2–1·5x0·5 µm) with single polar flagellum. Gram-negative cell wall structure. Anaerobic to microaerobic. Spores absent. Moderate thermophile, growing at 45–65 °C (optimum 55 °C). Neutrophile, growing at pH 6·5–7·4 (optimum pH 6·9–7·1). Grows in 5–50 g NaCl l-1 (optimum around 30 g NaCl l-1). Utilizes H2 as energy source, elemental sulfur, nitrate or oxygen as electron acceptors and CO2 as carbon source. Nitrate and sulfur are respectively reduced to ammonium and hydrogen sulfide in the course of growth. Growth is not supported by acetate, formate, butyrate, propionate, malate, succinate, methanol, ethanol, pyruvate, lactate, fumarate, methylamine, glucose, sucrose, starch, peptone or yeast extract. Acetate, pyruvate, formate, methylamine, methanol and malate cannot replace CO2 as carbon source. Sulfate, sulfite and thiosulfate are not utilized as electron acceptors. Grows in the presence of chloramphenicol and tetracycline (both at 100 µg ml-1). DNA G+C content of the type strain is 32·1 mol%.
The type strain, CRT (=DSM 15016T=JCM 11957T), was isolated from the content of a vent cap deployed in the Mid-Atlantic Ridge (23°N).
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ACKNOWLEDGEMENTS |
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REFERENCES |
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