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Allochromatium Vinosum DSM 180T

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Allochromatium Vinosum DSM 180T Standards in Genomic Sciences (2011) 5:311-330 DOI:10.4056/sigs.2334270 Complete genome sequence of Allochromatium vinosum DSM 180T Thomas Weissgerber1, Renate Zigann1, David Bruce2, Yun-juan Chang2, John C. Detter2, Cliff Han2, Loren Hauser2, Cynthia D. Jeffries2, Miriam Land2, A. Christine Munk2, Roxanne Tapia2, Christiane Dahl1* 1Institut für Mikrobiologie & Biotechnologie, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany 2DOE Joint Genome Institute, Walnut Creek, California, USA *Corresponding author: [email protected] Keywords: purple sulfur bacteria, Chromatiaceae, versatile Allochromatium vinosum formerly Chromatium vinosum is a mesophilic purple sulfur bacte- rium belonging to the family Chromatiaceae in the bacterial class Gammaproteobacteria. The genus Allochromatium contains currently five species. All members were isolated from fresh- water, brackish water or marine habitats and are predominately obligate phototrophs. Here we describe the features of the organism, together with the complete genome sequence and annotation. This is the first completed genome sequence of a member of the Chromatiaceae within the purple sulfur bacteria thriving in globally occurring habitats. The 3,669,074 bp ge- nome with its 3,302 protein-coding and 64 RNA genes was sequenced within the Joint Ge- nome Institute Community Sequencing Program. Dedicated to Prof. Dr. Hans G. Trüper, Bonn, on the occasion of his 75th birthday on March 16th, 2011, for his fundamental work on phototrophic sulfur bacteria. Introduction Anoxygenic purple sulfur bacteria are Gammapro- thiorhodospiraceae and the only very distantly teobacteria whereas chemotrophic sulfur- related green sulfur bacteria, members of the fam- oxidizing bacteria are found in four classes (Al- ily Chromatiaceae like A. vinosum store sulfur glo- phaproteobacteria, Betaproteobacteria, Gamma- bules inside of the cells when oxidizing sulfide or proteobacteria and Epsilonproteobacteria) of the thiosulfate. They have this trait in common with a Proteobacteria. Strain DSM 180T (= ATCC 17899 = large number of environmentally important che- D = NBRC 103801) is the type strain of the species motrophic sulfur oxidizers like Beggiatoa or the Allochromatium vinosum, which belongs to the sulfur-oxidizing bacterial symbionts of marine Chromatiaceae, one of currently five families in animals like Riftia pachyptila or Olavius algarven- the order Chromatiales. Species belonging to the sis. Anoxygenic purple sulfur bacteria are also families Chromatiaceae and Ectothiorhodospira- important primary producers of fixed carbon (up ceae are mainly anoxygenic photolithoautotrophic to 83% of primary production in lakes can be bacteria, which are able to oxidize various sulfur anoxygenic) [1]. The CO2 is fixed at the expense of compounds. Anoxygenic purple sulfur bacteria the energy derived from the virtually unlimited like A. vinosum flourish wherever light reaches and environmentally safe source of sunlight. Si- sulfidic water layers or sediments and often occur multaneous with the large scale conversion of CO2 as dense accumulations in conspicuous blooms in into organic compounds, purple sulfur bacteria freshwater as well as in marine aquatic ecosys- oxidize reduced sulfur compounds and use these tems. Here, they are major players in the reoxida- as photosynthetic electron donors [2]. In almost tion of sulfide produced by sulfate-reducing bacte- all freshwater and marine photic-anoxic environ- ria in deeper anoxic layers. In contrast to anox- ments, purple and also green sulfur bacteria ygenic purple sulfur bacteria of the family Ecto- represent the dominant anoxygenic phototrophs. The Genomic Standards Consortium Allochromatium vinosum DSM 180T Only very few and atypical ecosystems heavily marches or intertidal mud flats. Here we present a polluted with organic waste have been described summary classification and a set of features for A. in which phototrophic Alphaproteobacteria out- vinosum strain DSM 180T, together with the de- number purple sulfur bacteria. In addition to their scription of the complete genomic sequencing and environmental importance, purple sulfur bacteria annotation. like A. vinosum have a long tradition of biotechno- logical application not only in waste remediation Classification and features and removal of toxic compounds, e.g. odorous There are five described species currently belong- sulfur compounds like sulfide or even explosives ing to the genus Allochromatium [10, Table 1] [3-5], but also in the production of industrially namely A. vinosum, A. minutissimum, A. warmingii, relevant organochemicals such as vitamins or bio- A. phaeobacterium and A. renukae. Figure 1 shows polyesters [6-8] and the production of biohydro- the phylogenetic neighborhood of A. vinosum DSM gen [9]. 180T in a 16S rRNA based maximum likelihood Strains of all Allochromatium species were iso- phylogenetic tree. Based on 16S rRNA gene se- lated from freshwater, brackish water and marine quences the closest related type strain is A. minu- habitats. A. vinosum is environmentally abundant tissimum DSM 1376T with 98.4% sequence identi- and occurs not only in pelagic communities but ty, while the other type strains of the genus Al- also in littoral sediments like sandy beaches, salt lochromatium share 93.8-97% sequence identity. 100 Allochromatium vinosum DSM 180T 61 Allochromatium minutissimum DSM 1376T 92 Allochromatium renukae JA136T 76 100 Allochromatium phaeobacterium JA144T 100 100 Allochromatium warmingii DSM 173T T 100 Thermochromatium tepidum MC Thiocapsa roseopersicina 1711T T Halorhodospira halophila SL1 100 Halorhodospira abdelmalekii DSM 2110T Ectothiorhodospira haloalkaliphila BN 9903T 0.01 Figure 1. Phylogenetic tree highlighting the position of A. vinosum DSM 180T relative to several other type strains within the Chromatiaceae and Ectothiorhodospiraceae based on 16S rRNA sequence analysis. The tree was built with the RDP Tree Builder and numbers above branches are support values from 100 bootstrap replicates [25]. Bar, 1 nucleotide substitutions per 100 nucleotides. Cells of A. vinosum are Gram stain negative, rod A. phaeobacterium and A. warmingii produce rho- shaped and about 2.0 µm × 2.5–6 µm in size [Fig- dopinals and A. renukae lycopenes, respectively. ure 2]. There is a high intraspecies variation of the Optimal growth of A. vinosum is achieved within a G + C content within the genus Allochromatium. temperature range between 25-35 °C and a pH For example the G + C content of A. vinosum range between 7.0-7.3, respectively [21]. (64.3%) and A. warmingii (55.1-60.2%) differs up Most purple sulfur bacteria grow preferentially by to 10 mol % G + C content of the DNA. Cells of all photolithoautotrophic oxidation of reduced sulfur species are motile and contain internal membrane compounds. However, A. vinosum is an ecological- structures of a vesicular type. The main carotinoid ly significant, typically dominant inhabitant of synthesized by A. vinosum and A. minutissimum intertidal sediments, i.e. a fluctuating environment belongs to the group of spirilloxanthins, whereas in which redox conditions change rapidly within 312 Standards in Genomic Sciences Weissgerber et al. hours. A. vinosum has adapted to this environment Photoorganoheterotrophic growth occurs with and developed high metabolic versatility. While A. formate, acetate, propionate, butyrate, pyruvate, vinosum and A. minutissimum are capable of grow- fumarate, succinate, malate and glycolate as organ- ing both photolithotrophically and chemolitho- ic electron donors. At reduced oxygen partial pres- trophically the remaining species are obligate pho- sure even chemoorganoheterotrophic and chemoli- totrophs. Photolithoautotrophic growth of A. vino- thoautotrophic growth in the dark is possible with sum occurs with hydrogen, sulfide, polysulfide, oxygen as the terminal electron acceptor [26]. Un- thiosulfate, sulfur and sulfite as electron donors. der such conditions A. vinosum and A. minutissi- Light energy is used to transfer the electrons of mum assimilate sulfate. This versatility is not these different compounds to the level of the more shared by other anoxygenic phototrophic organ- highly reducing electron carriers NAD(P)+ and fer- isms like the green sulfur bacteria (Chlorobiaceae). redoxin for reductive carbon dioxide fixation. Figure 2. Transmission electron micrograph of a cell of A. vinosum strain 9011 (Photo kindly provided by Hans G. Trüper, Bonn). Magnification × 59,050. As a result of the preparation for electron microscopy, the localization of sulfur globules is visible as “holes” in the electron micrograph. Genome sequencing and annotation Genome project history This organism was selected for sequencing on the in 2 ml ice-cold TES buffer at pH 8. Cells were har- basis of its environmental abundance and impor- vested, mixed with 250 µl sucrose solution (20% tance, its capability to produce hydrogen and its (w/v) sucrose in TES) and incubated for 30 min accessibility by manipulative genetics for biotech- on ice. Afterwards, 250 µl of lysozyme RNAse solu- nology. The genome project is deposited in the tion (20 mg/ ml lysozyme, 1 mg/ ml RNAse) were Genomes OnLine Database [27] and the complete added followed by a further incubation for 30 min genome sequence is available in GenBank. Se- at 37 °C with gentle shaking. 100 µl sarcosine so- quencing, finishing and annotation were per- lution (10% (w/v) laurylsarcosine, 250 mM ED- formed by the DOE Joint Genome Institute (JGI). A TA) were added and the sample was
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