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Colwellia Demingiae Sp. Nov., Colwellia and Colwellia Psychrotropica Sp. Nov. international Journal of Systematic Bacteriology (1998), 48, 1 17 1-1 180 Printed in Great Britain ~ __ __ Colwellia demingiae sp. nov., Colwellia hornerae sp. nov., Colwellia rossensis sp. nov. and Colwellia psychrotropica sp. nov. : psychrophi Iic Antarctic species with the abi Iity to synthesize docosahexaenoic acid (22 :6~3) John P. Bowman,lI2 John J. Gosinkt3Sharee A. McCammon,’ Tom E. Lewis,’t2 David S. Nichols,’f2Peter D. Nich~ls,~~~Jenny H. Skerratt,’ Jim T. Staley3and Tom A. McMeekin1n2 Author for correspondence : John P. Bowman. Tel : + 6 I 3 6226 2776. Fax : + 61 3 6226 2642. e-mail: john.bowmaniu utas.edu.au I,* Antarctic CRC’ and As part of a general survey of the biodiversity and inherent ecophysiology of Depa rtme nt of bacteria associated with coastal Antarctic sea-ice diatom assemblages, eight Agricultural Sciencez, University of Tasmania, strains were identified by 165 rRNA sequence analysis as belonging to the GPO Box 252-80, Hobart, genus Colwellia. The isolates were non-pigmented, curved rod-like cells whieh Tasmania 7001, Australia exhibited psychrophilic and facultative anaerobic growth and possessed an Department of absolute requirement for sea water. One isolate was able to form gas vesicles. M icro bi o logy, Un iversity All strains synthesized the co3 polyunsaturated fatty acid (PUFA) of Washington, Seattle, WA 98195, USA docosahexaenoic acid (22 :6~3, DHA) (0*7-8.0% of total fatty acids). Previously, DHA has only been detected in strains isolated from deep-sea benthic and CSIRO Marine Research Division, Castray faunal habitats and is associated with enhanced survival in permanently cold Es p Ia nade, Ho ba rt, habitats. The G+C content of the DNA from the Antarctic Colwellia strains Tasmania, 7001, Australia ranged from 35 to 42 mol O/O and DNA-DNA hybridization analyses indicated that the isolates formed five genospecies, including the species Colwellia psychrerythraea (ACAM 550T). 16s rRNA sequence analysis indicated that the strains formed a cluster in the y-subclass of the Proteobacteria with Colwellia psychrerythraea. Sequence similarities ranged from 95.2 to 100 O/O between the various Antarctic Colwellia isolates. Phenotypic characterization confirmed distinct differences between the different genospecies. These studies indicate that the DHA-producing Antarctic isolates consist of five different Colwellia species: Colwellia psychrerythraea and four novel species with the proposed names Colwellia demingiae sp. nov. (ACAM 45gT), Colwellia psychrotropica sp. nov. (ACAM 1793. Colwellia rossensis sp. nov. (ACAM 608T)and Colwellia hornerae sp. nov. (ACAM 607T). Keywords : Antarctic sea ice, polyunsaturated fatty acids, docosahexaenoic acid, psychrophilic bacteria, Colivellin INTRODUCTION Suzuki et al., 1997) and from the Marianas Trench (DeLong & Yayanos, 1986). Phylogenetic analysis Colwelliu-related clones and isolates have been based on 5s (Deming et al.. 1984,1988) and 16s rRNA obtained from aggregates of particulate organic sequences (DeLong et al., 1993; Gosink & Staley, material and coastal marine water samples collected 1995; Bowman et al., 1997a) has indicated that this offshore of the United States (DeLong et a/., 1993; genus is most closely related to other Gram-negative marine genera such as Sheivnnella, Ferrimonas, . .. ., .. , , , , , ., , , . , . , , ., . , , . .. .. , , , ., . .. .. .. .. , , ., .. ,. .. , . , , , , ., . , . .. .. .. , . .. .. .. Abbreviations: DHA, docosahexaenoic acid (22: 6~3);EPA, eico- Pseudoalteromonus and .4lteromonas (Gauthier et a/., sapentaenoic acid (20: 5r~13);PUFA, polyunsaturated fatty acid; TMAO, 1995 ; Rossello-Mora et al., 1995). Species of the genus trimethylamine N-oxide. Colu~elliuare facultative anaerobes, characteristically 1171 J. P. Bowman and others psychrophilic (no growth at 20 OC, optimum growth at (Difco) or on R2A agar (Oxoid) prepared with sea water < 15 "C),sometimes barophilic and possess a require- salts (Ocean Nature, Aquasonic). ment for elevated sodium and magnesium ions to Phenotypic characterization. Most of the phenotypic tests maintain cell wall and cytoplasmic membrane integrity used in this study have been described previously (Bowman (D'Aoust & Kushner, 1972). Recent studies indicate c'f id., 1997b). Sodium, magnesium and calcium ion re- that strains of Colivellia and [ Vihrio]marinus synthesize quirement was tested in a basal medium derived from marine a3 polyunsaturated fatty acids (PUFAs), in particular 2216 agar containing (per litre distilled water) 5 g Bacto docosahexaenoic acid (22: 6~3,DHA) (DeLong & peptone, 2 g yeast extract and 10mg ferric phosphate. Chloride salts were tested at concentrations found typically Yayanos, 1986; DeLong et al., 1997). PUFAs such as in sea water: 0.4 M NaC1, 25 mM MgCI, and 8 mM CaCl, DHA and eicosapentaenoic acid (20: 523, EPA) are (ZoBell, 1946). essential for human and animal health in a variety of ways. For example, PUFAs are believed to lower the Dissimilatory iron reduction was tested in a medium adapted from Widdel & Bak (1992) and prepared using the Hungate levels of blood plasma cholesterol and triacylglycerols, technique (H ungate, 1968). The medium was prepared with prevent cardiovascular disease and reduce the risk of artificial sea water and contained 10 mM amorphic ferric some cancers (Kelly, 1991). They are also required for oxide/neutralized ferric chloride or 10 mM soluble ferric normal embryonic development, particularly optical oxide/ferric pyrophosphate (Lovely & Phillips, 1986) as the and neural development (Craigschmidt et ul., 1996 ; electron acceptors and 10 mM sodium acetate as the electron Farkas et al., 1996; Linko & Hayakawa, 1996). w3 donor and carbon source. Uninoculated controls lacking the PUFAs are important food supplements for rearing iron electron acceptors were also prepared. Iron reduction larval fish in the aquaculture industry. In most cases was confirmed by the appearance of a black precipitate fish obtain PUFA from 'live feed', including rotifers (magnetite) and by use of the Merckoquant Iron Test (Merck). or Arteniia spp. fed on PUFA-rich microalgae, or from PUFA-amended artificial feed (Ostrowski & Anaerobic growth with 10 mM trimethylamine N-oxide Divakaran, 1990; Southgate & Lou, 1995). Bacteria (TMAO) was tested in mineral salts medium containing (per are recognized as an alternative source of PUFAs for litre sea water) 2 g ammonium chloride, 2 mM potassium phosphate buffer, pH 7.0, 2 ml SL- 10 trace element solution the development of less expensive aquaculture fish (Overmann & Pfennig, 1989), 1 g yeast extract and 10 ml feeds (Nichols et al., 1996). vitamin solution no. 6 (Staley ct d.,1992). The medium pH Currently, the genus Colwellin contains two species : was adjusted to 7.0 using 1 M KOH and was solidified with 1.3 '/o (w/v) purified agar (Oxoid). Sodium acetate (20 mM) Coltv elliu psyclz r oery tli r us and Colit vllia hadaliens is was used as the electron donor and carbon source. Plates (Deming et a/., 1988). Colivcllia ps~~clzroer~t1zrri.swas were incubated in an anaerobic jar using Anaerogen named following the observation that the species Gaspaks (Oxoid). Growth on the plates was compared with ' Vihrio psvchroery thrus' (D'Aoust & Kushner, 1972) control plates lacking TMAO. was phylogenetically distinct from the rest of the genus Additional biochemical tests were performed using the API Vihrio (Deming et a/., 1988). The obligately barophilic 20E test kit (bioMerieux) prepared according to the manu- species Colivellia /iadulier?sis was also described at that facturer's specifications except that bacterial strains were time. The epithet psychroerythrus has been changed to suspended in chilled artificial sea water. Carbon and energy psi,chrc.ri,thrueu (L. adj. erjJthraeus -a, -um red) as the source screening utilized a 0.1 '/o concentration of test name Colivelliu is feminine (Euzeby, 1998). compounds, except carbohydrates, which were tested at a concentration of 0.2%. The basal medium used was the Recently, it was found that a number of Antarctic fast same as for the TMAO reduction test. Media lacking a sea-ice isolates and a single strain from an Antarctic carbon source were prepared as negative controls to account meromictic marine salinity lake belonged to the genus for any background growth. Cohvelliu (Bowman et al., 1997a). In addition, a gas- Growth rate analysis. The growth rates of strains ACAM vesicle-forming isolate from the ice/water interface 605, ACAM 607T and ACAM 179' were determined in a of sea ice in McMurdo Sound, Antarctica, was temperature gradient incubator (Toyokagaku Sangyo). The also shown to be closely related to Colitdlia temperature gradient used ranged from 0 to 20-27 "C and psychrerythruea (Gosink & Staley, 1995). In this study, tubes, containing 10 ml marine 2216 broth, were inoculated these isolates were investigated and found to represent with 0.5 ml cells taken from cultures in late-exponential several novel species of the genus Colivelliu : Coltvellin growth phase. Growth was measured by a decrease in denzingiao sp. nov., Cohvellia rossemis sp. nov., transmittance at 550 nm for up to 14d. Growth was Colivelliu hornerae sp. nov. and Colwellia ps~*cliro- considered to have occurred if the culture transmittance tropicu sp. nov. All species of the genus Colit*ellia were decreased by more than 20%. The data were fitted to the square-root growth model of Ratkowsky ct nl. (1983) and found to form DHA, the level of which increases with cardinal temperatures determined. decreasing optimum growth
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