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Shewanella Amazonensis Sp. Nov., a Novel Metal-Reducing Facultative Anaerobe from Amazonian Shelf Muds

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Shewanella Amazonensis Sp. Nov., a Novel Metal-Reducing Facultative Anaerobe from Amazonian Shelf Muds International Journal of Systematic Bacteriology (1998),48,965-972 Printed in Great Britain Shewanella amazonensis sp. nov., a novel metal-reducing facultative anaerobe from Amazonian shelf muds Kasthuri Venkate~waran,'~~Michael E. Dollhopf,' Robert Aller,' Erko Stackebrandt3and Kenneth H. Nealson' Author for correspondence: Kasthuri Venkateswaran. Tel: + 1 626 395 2994. Fax: + 1 626 395 2940. e-mail : kjvenkat @cco .caltech.edu 1 Center for Great Lakes A new bacterial species belonging to the genus Shewanella is described on the Studies, University of basis of phenotypic characterization and sequence analysis of its 165 rRNA- Wisconsi n-Milwau keel Milwaukee, WI 53204, USA encoding and gyrase B (gyrB) genes. This organism, isolated from shallow- water marine sediments derived from the Amazon River delta, is a Gram- 2 Marine Sciences Research Center, State University of negative, motile, polarly flagellated, facultatively anaerobic, rod-shaped New York, Stony Brook, eubacterium and has a G+C content of 51.7 mol0/o. Strain SB2BTis exceptionally NY 11794-5000, USA active in the anaerobic reduction of iron, manganese and sulfur compounds. 3 DSMZ, Mascheroder Weg SB2BTgrows optimally at 35 "C, with 1-3% NaCl and over a pH range of 7-8. 1b, D-38124 Braunschweig, Analysis of the 165 rDNA sequence revealed a clear affiliation between strain Germany SB2BTand members of the gamma subclass of the class Proteobacteria. High 4 California Institute of similarity values were found with certain members of the genus Shewanella, Technology, Dept of Environmental especially with Shewanella putrefaciens, and this was supported by cellular Engineering, 1200 E. fatty acid profiles and phenotypic characterization. DNA-DNA hybridization California Blvd, Mail Code between strain SB2BTand its phylogenetically closest relatives revealed low 138-78, Pasadena, CA 91 125, USA similarity values (246-4207%) which indicated species status for strain SB2BT. That SB2BTrepresents a distinct bacterial species within the genus Shewanella is also supported by gyrB sequence analysis. Considering the source of the isolate, the name Shewanella amazonensis sp. nov. is proposed and strain SB2BT(= ATCC 7003293 is designated as the type strain. Keywords : Shewanella amazonensis sp. nov., metal reduction, gamma Proteobacteria, 16s rRNA, DNA gyrase INTRODUCTION respiratory growth to the reduction of metals was Shewanella putrefaciens (Meyers & Nealson, 1988). Biogeochemical data have long suggested a significant role for iron and manganese reduction in global In this paper we describe the isolation of a new metal- nutrient cycling. In recent years, a number of dis- reducing bacterium of the genus Shewanella from similatory metal-reducing bacteria have been de- shallow-water marine deposits derived largely from scribed (see review by Nealson & Safarini, 1994), and the Amazon River delta off the Amapa coast of Brazil. a role for such micro-organisms as catalysts of both The Amazon River delta is one of the major sediment manganese and iron reduction in natural systems has depocentres on Earth (- 3-6% of global riverine been inferred. One of the first bacteria shown to link its sediment supply), and is characterized by unusally extensive zones of sedimentary Fe and Mn cycling Abbreviation: FAME, fatty acid methyl ester. (Aller et al., 1986, 1996, 1997; Allison et al., 1995; The GenBank accession numbers for the nucleotide sequences in this paper Kuehl et al., 1986). The upper 1-2 m of delta topset are: 5. amazonensis ATCC 70032gT- AF005257 (gyrB) and AF005248 (165 deposits, encompassing a mass of - 20-30 x lo9metric rDNA); S. algae ATCC 51 192T- AF005686 (gyrB) and AF005249 (165 rDNA); tonnes of sediment, are dominated by non-sulfidic, 5. benthica ATCC 43992T gyrB, AF014949; S. hanedai ATCC 33224T gyrB, suboxic redox conditions, with pore-water-dissolved AF005693; S. frigidimarina ACAM 591T gyrB, AF014947; 5. gelidimarina ACAM 456TgyrB, AF014946; 5. putrefaciens ATCC 8071TgyrB, AF005669; S. Fe2+ concentrations typically ranging from - 0.1- woodyi ATCC 51908T gyrB, AF014944; Shewanella sp. ANG-SQl gyrB, 1 mM. Samples from the seasonally mobile inter- AFO 14945. tidal deposits at the initiation of this coastal system 00766 0 1998 IUMS 965 K. Venkateswaran and others south of Cab0 Cassipork were obtained for the present marina ACAM 456T, were received from the University of study. Tasmania, Australia. All strains were maintained in semi- solid nutrient agar (Difco) and bench cultures were made in Strain SB2BT was isolated from Amazonian shelf either LB liquid or agar media (Sambrook et al., 1989). coastal muds, and is a highly active reducer of iron and Growth conditions. Strain SB2BTwas cultured aerobically in manganese oxides, thiosulfate and elemental sulfur. LB liquid medium, and either 10 M HCl or 10% (w/v) Bacterial isolates showing the properties of Gram- NaOH were used to obtain a pH range from 5 to 10. Cultures negative motile rods with positive oxidase and catalase inoculated in LB liquid medium (pH 7) were incubated at reactions, strict respiratory metabolism, ability to various temperatures under aerobic conditions. The effects reduce a variety of electron acceptors, including of various concentrations of NaCl (0-10 YO)were studied trimethylamine N-oxide (TMAO), and production of using 1% Bacto-tryptone (Difco) as the basal medium. hydrogen sulfide (Stenstrom & Molin, 1990) have until Growth was monitored at appropriate intervals by OD,,, recently been placed under S. putrefaciens. Shewanella measurements with a visible-light spectrophotometer (LKM was established around its type species S. putrefaciens Biochrom Ultrospec 4050). Anaerobic growth was ac- complished in an anaerobic chamber (Coy Laboratory and included Shewanella hanedai (Jensen et al., 1980) Products) maintained at 2% hydrogen, the balance in and Shewanella benthica (MacDonnell & Colwell, nitrogen. 1985). Simidu et al. (1990) described Shewanella alga For visualizing cell shape and flagella, cells were negatively [corrected to Shewanella algae (Truper & de' Clari, stained with osmium chloride according to the methods of 1997)] as mesophilic, and relatively high in G+C% Cole & Popkin (1981) and then observed with an Hitachi content. On the basis of whole-cell protein profiles, H-600 transmission electron microscope. ribotyping and 16s rRNA-encoding gene sequence Isolation of metal-reducing bacteria. A population of metal- analysis, S. algae was recently phylogenetically charac- reducing bacteria was enriched as described previously terized (Fonnesbech-Vogel et al., 1997). (Nealson et al., 1991). Briefly, sediment was mixed with an Conventional phenotypic and chemotaxonomic analy- equal volume of 1.5 YOagar containing LM medium supple- ses identified strain SB2BTas S. putrefaciens. However, mented with carbon substrate {O-02YO yeast extract, 0.01 % peptone, 0.6 NaCl, 10 mM sodium bicarbonate, 10 mM designed YO PCR probes to recognize S. putrefaciens HEPES, 5 mM lactate, 5 mM succinate, 5 mM glycerol, based on gyrB (encoding the B subunit of DNA 1 mM acetate, 0.5 mM ferric chloride, 5 mM sodium mol- gyrase, topoisomerase 11) failed to generate a specific ybdate and ferrozine [3-(2-pyridyl)-5,6 bis (4-phenylsulfonic amplicon for SB2BT (data not shown), suggesting that acid)-1,2,4 triazine], pH 7.2). The vials were sealed off from this strain may represent a new species. To elucidate oxygen and incubated at room temperature; they were the phylogenetic status of SB2BT, its 16s rDNA and monitored daily and scored qualitatively for iron reduction. gyrB gene sequences were analysed. Both sequences After a secondary enrichment, samples that showed zones of differ from all known shewanellae, suggesting that the strong metal reduction were streaked onto plates with similar organism does indeed deserve the status of new species. media, substituting 50 mM ferric citrate for the ferric chloride to isolate single colonies. Appropriate positive (Shewanella sp. MR- 1) and negative (Escherichia coli ATCC METHODS 25922) controls were performed. Since anaerobic sulfur Sample collection. Strain SB2BTwas isolated from relatively reduction appears to be a trait associated with the Shewanella low salinity (pore water C1- - 0-1-0.2 mM), mud flat species (Moser & Nealson, 1996), analysis was carried out as sediment obtained in - 1 m water, a few kilometres south of per the protocols delineated by Moser & Nealson (1 996). Cab0 Cassipore, Amapi, Brazil, on 12 March 1996 (Station Measurement of metal reduction. LM growth medium SB2B, 03" 52.59' N, 51" 04-30' W). At the time of collection, containing 0.6% NaCl and 20 mM lactate (Meyers & surface pore-water salinities were relatively low, C1- - 0.1- Nealson, 1988) was used for metal reduction experiments. 0.2mM, but as indicated by the activity of the naturally Amorphous manganese oxide (Lovely & Phillips, 1988) and occurring radionuclide 234Th(tl,2 = 24.1 d), these deposits FeOOH (Atkinson et al., 1967) were prepared as described frequently exchange with regions offshore, and thus ex- elsewhere. Inocula were grown aerobically in LB liquid perience a wide range of salinities over weekly timescales. medium at 30 "C, harvested by centrifugation, and adjusted Pore-water-transport models indicate that the upper few to an inoculum size of approximately 2.0 x lo7(equivalent to decimetres of sediment are physically mixed by waves and OD,,, = 0.2) bacterial cells per ml in LM medium containing currents over timescales of < 1 week. Sediment cores were either ferric or manganese oxides. All media and solutions taken manually using CAB tubing (1 5.2 cm o.d.), the upper were de-aerated by purging with nitrogen prior to the - 50 cm was placed in 500 ml polyethylene bottles, and then experiment. Samples (500 pl) were drawn at 30 min intervals, stored in larger wide-mouth glass jars filled with sediment passed through a 0.2 pm filter (Millipore) and the resulting from the same site. Intertidal surface water temperatures soluble (reduced) metal was measured by atomic absorption along the coast ranged from - 26-4-315 "C. Sediment was spectrometry (Burdige & Nealson, 1986). To determine total kept at - 28 "C except during - 2 d transport (4 "C).
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