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Chromohalobacter Salexigens Type Strain (1H11T) Alex Copeland1, Kathleen O’Connor2, Susan Lucas1, Alla Lapidus1, Kerrie W

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Chromohalobacter Salexigens Type Strain (1H11T) Alex Copeland1, Kathleen O’Connor2, Susan Lucas1, Alla Lapidus1, Kerrie W Standards in Genomic Sciences (2011) 5:379-388 DOI:10.4056/sigs.2285059 Complete genome sequence of the halophilic and highly halotolerant Chromohalobacter salexigens type strain (1H11T) Alex Copeland1, Kathleen O’Connor2, Susan Lucas1, Alla Lapidus1, Kerrie W. Berry1, John C. Detter1,3, Tijana Glavina Del Rio1, Nancy Hammon1, Eileen Dalin1, Hope Tice1, Sam Pit- luck1, David Bruce1,3, Lynne Goodwin1,3, Cliff Han1,3, Roxanne Tapia1,3, Elizabeth Saund- ers1,3, Jeremy Schmutz3, Thomas Brettin1,4 Frank Larimer1,4, Miriam Land1,4, Loren Hauser1,4, Carmen Vargas5, Joaquin J. Nieto5, Nikos C. Kyrpides1, Natalia Ivanova1, Markus Göker6, Hans-Peter Klenk6*, Laszlo N. Csonka2*, and Tanja Woyke1 1 DOE Joint Genome Institute, Walnut Creek, California, USA 2 Department of Biological Sciences, Purdue University, West Lafayette, Indiana, USA 3 Los Alamos National Laboratory, Bioscience Division, Los Alamos, New Mexico, USA 4 Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA 5 Department of Microbiology and Parasitology, University of Seville, Spain 6 Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany *Corresponding authors: [email protected], [email protected] Keywords: aerobic, chemoorganotrophic, Gram-negative, motile, moderately halophilic, halo tolerant, ectoine synthesis, Halomonadaceae, Gammaproteobacteria, DOEM 2004 Chromohalobacter salexigens is one of nine currently known species of the genus Chromoha- lobacter in the family Halomonadaceae. It is the most halotolerant of the so-called ‘mod- erately halophilic bacteria’ currently known and, due to its strong euryhaline phenotype, it is an established model organism for prokaryotic osmoadaptation. C. salexigens strain 1H11T and Halomonas elongata are the first and the second members of the family Halomonada- ceae with a completely sequenced genome. The 3,696,649 bp long chromosome with a total of 3,319 protein-coding and 93 RNA genes was sequenced as part of the DOE Joint Genome Institute Program DOEM 2004. Introduction Strain 1H11T (= DSM 3043 = ATCC BAA-138 = known for its very broad salinity range [1] and for CECT 5384) is the type strain of the species Chro- its role as a model organism for prokaryotic os- mohalobacter salexigens [1], which is one of cur- mosadaptation [5-7], e.g. the synthesis of ectoines rently nine species in the genus Chromohalobacter (ectoine and hydroxyectoine) for cell stress pro- [1,2]. The genus name was derived from the Greek tection [8,9]. Here we present a summary classifi- words chroma, color, hals halos, salt, and the Neo- cation and characteristics of C. salexigens 1H11T, Latin bacter, rod, meaning the colored salt rod. together with the description of the complete ge- The species epithet originated from the Latin nomic sequencing and annotation. words sal salis, salt, and exigo, to demand; salt- demanding [3]. Strain 1H11T was originally iso- Classification and features lated in 1974 in Bonair, Netherlands Antilles, from The sequences of the five identical 16S rRNA genes salterns containing 18.6% salt, and was initially of strain 1H11T were compared using NCBI BLAST published as a strain belonging to the species Ha- [10] under default settings (e.g., considering only the lomonas elongata [4]. In 2001, Arahal et al. trans- high-scoring segment pairs (HSPs) from the best ferred the strain to the genus Chromohalobacter 250 hits) with the most recent release of the Green- [2] as the type strain of the then novel species C. genes database [11] and the relative frequencies of salexigens [1] following detailed phenotypic, geno- taxa and keywords (reduced to their stem [12]) typic, and phylogenetic analyses. C. salexigens is were determined and weighted by BLAST scores. The Genomic Standards Consortium Chromohalobacter salexigens type strain (1H11T) The most frequently occurring genera were Halo- identity of 100.0% and an HSP coverage of 100.0%. monas (50.7%), Chromohalobacter (46.3%), The most frequently occurring keywords within the 'Haererehalobacter' (1.7%), Bacillus (0.8%) and labels of environmental samples which yielded hits Pseudomonas (0.5%) (214 hits in total). For 16 hits were 'soil' (12.1%), 'lake' (3.6%), 'salin' (3.0%), to sequences from members of the C. salexigens spe- 'agricultur' (2.9%) and 'alkalin, chang, flood, former, cies, the average identity within HSPs was 99.9% mexico, texcoco' (2.6%) (36 hits in total). The most and the average coverage by HSPs was 97.9%. For frequently occurring keyword within the labels of 22 hits to sequences from other members of the ge- environmental samples which yielded hits of a high- nus Chromohalobacter, the average identity within er score than the highest scoring species was 'aquat, HSPs was 98.2% and the average coverage by HSPs harbour, newport, rank' (25.0%) (2 hits in total). was 98.6%. Among all other species, the one yielding These keywords fit reasonably well with the ecolog- the highest score was Chromohalobacter marismor- ical and physiological properties reported for strain tui (X87222), which corresponded to an identity of 1H11T in the original description [1]. 99.9% and an HSP coverage of 100.0%. (Note that Figure 1 shows the phylogenetic neighborhood of C. the Greengenes database uses the INSDC (= salexigens in a 16S rRNA based tree. The sequences EMBL/NCBI/DDBJ) annotation, which is not an au- of the five identical 16S rRNA gene copies in the ge- thoritative source for nomenclature or classifica- nome differ by two nucleotides from the previously tion.) The highest-scoring environmental sequence published 16S rRNA sequence (AJ295146), which was EU799899 ('It's all ranking aquatic Newport contains three ambiguous base calls. Harbor RI clone 1C227569'), which showed an Figure 1. Phylogenetic tree highlighting the position of C. salexigens relative to the type strains of the oth- er species within the genus and the type species of the other genera within the family Halomonadaceae. The tree was inferred from 1,440 aligned characters [13,14] of the 16S rRNA gene sequence under the maximum likelihood (ML) criterion [15]. Rooting was done initially using the midpoint method [16] and then checked for its agreement with the current classification (Table 1). The branches are scaled in terms of the expected number of substitutions per site. Numbers adjacent to the branches are support values from 1,000 ML bootstrap replicates [17] (left) and from 1,000 maximum parsimony bootstrap replicates [18] (right) if larger than 60%. Lineages with type strain genome sequencing projects registered in GOLD [19] are labeled with one asterisk, those also listed as 'Complete and Published' with two asterisks [20]. 380 Standards in Genomic Sciences Copeland et al. Cells of C. salexigens strain 1H11T are straight or moprotectants, such as glycine betaine or its pre- slightly curved rods, 0.7 to 1.0 by 2 to 3 µm in size cursor, choline [4,6,33]. In the complex medium (Figure 2) with squared ends and occur singly or in SW (‘sea water’), which is routinely used for grow- pairs [1,4]. Cells of strain 1H11T stain Gram- ing this type of microorganism, strain 1H11T negative, are motile with polar flagella, strictly grows optimally at 7.5 to 10% (w/v) NaCl, with aerobic, and are non-spore-forming [1,4]. Carbon growth occurring over the range of 0.9% to 25% and nitrogen source utilization and biochemistry of NaCl [1]. In casein medium, which was initially the strain were reported by Arahal et al. [1]. A par- used for strain isolation, growth occurs in the tial characterization of the carbon-source utiliza- presence of 32% solar salts [4]. In SW medium tion by the organism has also been presented by containing 10% (w/v) total salts, C. salexigens Csonka et al. [36], who reported that the strain can 1H11T can grow at a pH range from 5 to 10, with degrade a number of aromatic compounds, includ- an optimum at pH 7.5 [1]. In the same medium, ing benzoate, protocatechuate, 4-hydroxybenzoate, the temperature range for growth is 15 – 45°C, and toluene. with an optimum at 37°C [1]. In the standard de- C. salexigens 1H11T is a halophile, which according fined medium M63, supplemented with glucose as to the classification proposed by Kushner [37], is the sole carbon source, growth is optimal at 8.7 to on the borderline between "moderate" halophiles 11.6% NaCl but occurs over the range of 2.9% (those growing optimally between 2.9 -14.5% NaCl or a maximum of 19% NaCl [6]. Interestingly, NaCl) and "extreme" halophiles (those growing C. salexigens 1H11T exhibits maximal growth rate optimally between 8.7 -23.2% NaCl). In addition, it in glucose-M63 with only 1.8% (0.3M) NaCl in the displays extraordinarily high halotolerance (con- presence of high concentrations of salts of other sidered as the ability to live and survive under inorganic ions, including K+, Rb+, NH4+, Br-, NO3-, or - high salt concentrations), and is able to grow at SO4 [38]. However, it is an open question whether salt concentrations over 17.4% and 32% in de- this strain is unique among halophiles in being fined and complex media, respectively. However, able to use other inorganic ions in addition to Na+ both the minimum NaCl requirement and the up- and Cl- for maximal growth rate. per limit of NaCl tolerance are dependent on growth medium and temperature. The organism Chemotaxonomy can tolerate higher NaCl concentrations in LB or in Data on the structure of the cell wall, fatty acids other complex media than in defined media. In lipid composition, quinones and polar lipids are defined media, halotolerance is enhanced by os- not available. Figure 2. Light microscopic image of C. salexigens 1H11T http://standardsingenomics.org 381 Chromohalobacter salexigens type strain (1H11T) Table 1. Classification and general features of C. salexigens according to the MIGS recommendations [21].
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