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Amphipholis Squamata MICHAEL P APPLIED AND ENVIRONMENTAL MICROBIOLOGY, Aug. 1990, p. 2436-2440 Vol. 56, No. 8 0099-2240/90/082436-05$02.00/0 Copyright C) 1990, American Society for Microbiology Description of a Novel Symbiotic Bacterium from the Brittle Star, Amphipholis squamata MICHAEL P. LESSERt* AND RICHARD P. BLAKEMORE Department of Microbiology, University of New Hampshire, Durham, New Hampshire 03824 Received 8 November 1989/Accepted 3 June 1990 A gram-negative, marine, facultatively anaerobic bacterial isolate designated strain AS-1 was isolated from the subcuticular space of the brittle star, Amphipholis squamata. Its sensitivity to 0/129 and novobiocin, overall morphology, and biochemical characteristics and the moles percent guanine-plus-cytosine composition of its DNA (42.9 to 44.4) suggest that this isolate should be placed in the genus Vibrio. Strain AS-1 was not isolated from ambient seawater and is distinct from described Vibrio species. This symbiotic bacterium may assist its host as one of several mechanisms of nutrient acquisition during the brooding of developing embryos. The biology of bacterium-invertebrate symbiotic associa- isopropyl alcohol for 30 s and two rinses in sterile ASW. tions has elicited considerable interest, particularly since the Logarithmic dilutions were plated on Zobell modified 2216E discoveries during the past decade of chemoautotrophic medium (ASW, 1 g of peptone liter-1, 1 g of yeast extract symbiotic bacteria associated with several invertebrate spe- liter-' [pH 7.8 to 8.4]) (29), as were samples of ambient cies in sulfide-rich habitats (4, 5). Bacterial-invertebrate seawater from the site of collection and ASW controls. All symbioses (mutualistic) have been reported from many materials and equipment were sterilized, and all procedures invertebrate taxa, examples of which include cellulolytic were performed by aseptic techniques. Plates incubated nitrogen-fixing bacteria from the wood-boring bivalves of the aerobically at 20°C were examined daily, and numbers of family Teridinidae (28), methanogenic bacteria of protozoa CFU were determined by standard methods. 2216E medium (25, 26), methanotrophic bacteria of bivalves (6, 7), and was used throughout the study unless otherwise indicated. bacterial symbionts of echinoderms (11, 15). Experimental Electron microscopy. For transmission electron micros- evidence suggests many of these bacterial endosymbionts copy, whole animals were fixed (with glutaraldehyde and provide organic carbon to their hosts (3, 4, 12), as has been osmium tetroxide) by the method of Walker (27) and stained recently shown for the gutless bivalves Solemya velum and with uranyl acetate and lead citrate. Thin sections were Solemya reidi (8, 13). examined with a JEOL 200S transmission electron micro- Amphipholis squamata (Echinodermata: Ophiuroidea) is a scope operated at 80 kV. Bacterial isolates from A. squa- small (3- to 5-mm adult disk diameter), viviparous, and mata were fixed, negatively stained with uranyl acetate, and hermaphroditic brittle star that has symbiotic bacteria asso- examined as described above. ciated with its protective cuticle and the epithelial cells DNA extraction and base composition. The moles percent which secrete the cuticle (Fig. 1) (27a). Holland and Nealson guanine-plus-cytosine (G+C) content of DNA, extracted as (17) have shown by electron microscopy the presence of described by Marmur (22), was determined by the method of bacteria associated with cuticle-secreting epithelial cells in Marmur all five classes of echinoderms, but no isolation or charac- and Doty (23). Standards included DNA extracted terization of these bacteria has been done. We present here from Pseudomonas aeruginosa (ATCC 10145), Vibrio fis- a preliminary description of a gram-negative, facultatively cheri (ATCC 7744) (Photobacteriumfischeri) (19), and Esch- anaerobic, symbiotic bacterium isolated from the subcutic- erichia coli (ATCC 12435) which have moles percent G+C ular space ofA. squamata. This bacterium, designated strain values of 67, 41, and 51, respectively. AS-1, appears to be an undescribed Vibrio species. On the Temperature range of growth. The range of temperatures basis of the strong specific binding and localization of both supporting growth was determined in 250-ml Erlenmeyer the isolated bacterium and bacteria in situ with polyclonal flasks, each containing 125 ml of 2216E broth prepared with antibodies in an immunoperoxidase procedure (27a), it is 75% ASW and incubated at 4, 20, 30, 37, or 40°C for 14 days. likely that only strain AS-1 is present in the subcuticular Media were inoculated with 3 ml of a culture growing space. A description of the cellular interactions of the host exponentially at 20°C. Results were scored as positive or and negative on the basis of the presence of turbidity, which symbiont is presented elsewhere (27a). indicated growth in a particular medium. MATERIALS AND METHODS Salinity range of growth. The range of salinities supporting growth and the requirement for Na+ were determined in a Isolation and culture conditions. Freshly collected brittle manner similar to that of the temperature range. 2216E broth stars were maintained at 1 to 20°C, depending on the season was prepared with sterile distilled water (as opposed to of collection. Within 24 h of collection, whole, intact animals ASW) and adjusted with NaCl or KCI to final concentrations were homogenized in sterile 75% artificial seawater (ASW) of 0.0, 0.5, 1.0, 2.0, 2.5, 3.0, 3.5, 4.0, 6.0, 8.0, and 10.0% (18) with a glass tissue grinder after immersion in 70% (wt/vol). Antibiotic and inhibitor sensitivities. A saturated solution * Corresponding author. (10 ,ul) of 2,4-diamino-6,7-isopropylpteridine phosphate t Present address: Bigelow Laboratory for Ocean Sciences, (vibriostatic agent 0/129) in water was prepared on a sterile McKown Point, West Boothbay Harbor, ME 04575. paper disk and then placed in the center of an agar plate after 2436 VOL. 56, 1990 ECHINODERM-SYMBIOTIC BACTERIUM 2437 FIG. 1. Thin section of the bursal area ofA. squamata showing the relationship of numerous endosymbiotic bacteria (B) to the bursa (Bu), cuticle (C), and epithelial cells (E). Transmission electron microscopy was used for this figure. Bar = 3.0 ,.m. the plate was covered with cells of strain AS-1 from an RESULTS exponentially growing culture. Sterile antibiotic sensitivity disks (Difco Laboratories, Detroit, Mich.) were used to Morphology and ultrastructure. Translucent to opaque 1- determine novobiocin sensitivity (5 ,ug per disk). to 2-mm colonies of a single morphological type appeared The sensitivity to 1% (wt/vol) oxgall bile and 0.008% after 10 to 14 days on plates streaked with serial dilutions of (wt/vol) KCN was determined on 2216E agar. Results were homogenized whole animals. These colonies were mucoid, scored as positive or negative growth after 14 days (24). smooth, and convex with entire borders. Gram stains of the Biochemical tests. Preliminary biochemical tests were con- cells from these colonies revealed rod-shaped and comma- ducted with the API 20E system (Analytab Products, Plain- shaped gram-negative organisms averaging 0.7 by 1.6 ,um. view, N.Y.) inoculated as recommended by MacDonell et al. Spheroplasts formed in late-stationary-phase cultures as (20) for marine isolates. These tests were repeated on all reported for other species of the genus Vibrio (1, 2). isolates by standard techniques modified for marine bacteria The number of CFU per entire adult brittle star ranged (21, 24). Hugh-Liefson medium was made with 75% ASW from 5 x 106 to 9 x 106. All ASW controls produced no and supplemented with 1% glucose or mannitol, with bro- colonies, and colonies of similar characteristics, although mothymol blue as an indicator of fermentative metabolism. repeatedly sought, were never isolated from ambient seawa- The presence of cytochrome oxidase, catalase, coagulase, ter. Isolates of the same colony type were obtained in 10 urease, lipase, phosphatase, and sulfatase were determined separate isolation attempts, and all isolates were positive according to the methods of Smibert and Krieg (24) and with each other and the bacteria in situ by an immunoper- MacFaddin (21). oxidase assay (27a). Bacteria isolated from the brittle star Luminescence was examined by inoculating photobacte- homogenate were used as an antigen to produce polyclonal rium broth (Difco) under aerobic conditions at 20°C. Growth antibodies. These antibodies were then used as the primary and luminescence were determined daily for 14 days with V. antibody in the immunoperoxidase testing. Walker and fischeri (ATCC 7744) as a control. Lesser (27a) used tissue sections of the brittle star and the Hydrolysis of sodium hippurate, 0.1% (wt/vol) esculin, cultured bacteria in their assays. Appropriate controls and soluble starch, 12% gelatin, and cellulose was determined preabsorption of the antisera with E. coli to remove antibod- after 14 days of growth. Hydrogen sulfide production from ies against common antigens of the members of the family 0.03% sodium thiosulfate, indole production from 0.1% Enterobacteriaceae were used before any testing. These tryptophan, and acetoin production from glucose were de- isolates were maintained for more than a year on 2216E agar, termined after 14 days of growth (24). with the only detectable change being an increase in the Motility was determined by dark-field microscopy (hang- growth rate (M. P. Lesser, M.S. thesis, University of New ing drops) and motility test medium (Difco) made with 75% Hampshire, Durham, 1985). Occasional isolates from the A. ASW. squamata homogenate, morphologically resembling cells of Nitrate reduction was determined aerobically and anaer- the genus Flavobacterium, composed less than 1% of the obically with nitrate broth and nitrate agar (Difco) made with total colony counts in any isolation of the symbiotic bacteria 75% ASW. in which they appeared. 2438 LESSER AND BLAKEMORE APPL. ENVIRON. MICROBIOL. FIG. 2. (a) Thin section ofA. squamata showing a subcuticular symbiotic bacterium within a pocket formed by the epithelial cell. (b) Thin (cross) section of a symbiotic bacterium showing the features of the gram-negative envelope.
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