Open Access

The complete genome sequences of sulfur-oxidizing Gammaproteobacteria Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T

  • Kazuhiro Umezawa1,
  • Tomohiro Watanabe1,
  • Aya Miura1,
  • Hisaya Kojima1Email author and
  • Manabu Fukui1
Standards in Genomic Sciences201611:71

https://doi.org/10.1186/s40793-016-0196-0

Received: 4 August 2016

Accepted: 7 September 2016

Published: 15 September 2016

Abstract

Sulfurifustis variabilis and Sulfuricaulis limicola are autotrophic sulfur-oxidizing bacteria belonging to the family Acidiferrobacteraceae in the order Acidiferrobacterales. The type strains of these species, strain skN76T and strain HA5T, were isolated from lakes in Japan. Here we describe the complete genome sequences of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T. The genome of Sulfurifustis variabilis skN76T consists of one circular chromosome with size of 4.0 Mbp including 3864 protein-coding sequences. The genome of Sulfuricaulis limicola HA5T is 2.9 Mbp chromosome with 2763 protein-coding sequences. In both genomes, 46 transfer RNA-coding genes and one ribosomal RNA operon were identified. In the genomes, redundancies of the genes involved in sulfur oxidation and inorganic carbon fixation pathways were observed. This is the first report to show the complete genome sequences of bacteria belonging to the order Acidiferrobacterales in the class Gammaproteobacteria.

Keywords

Bacteria Gram-negative Sulfur-oxidizing bacteria Acidiferrobacterales Acidiferrobacteraceae

Introduction

Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T are gammaproteobacterial sulfur-oxidizing bacteria isolated from sediments of Lake Mizugaki and Lake Harutori, respectively [1, 2]. They both belong to the family Acidiferrobacteraceae in the order Acidiferrobacterales . In this order, only three species have been isolated in pure culture. They are all chemolithoautotrophs and can grow by oxidation of inorganic sulfur compounds. Sulfurifustis variabilis and Sulfuricaulis limicola are neutrophilic, whereas the other species, Acidiferrobacter thiooxydans , is acidophilic [3]. Taxonomy of Acidiferrobacter thiooxydans has been revised several times, and the family Acidiferrobacteraceae and order Acidiferrobacterales were recently established to accommodate the species [1, 35]. The members of the family Acidiferrobacteraceae have been frequently detected in various environments as gene sequences [2, 3, 6].

Here we show the complete genome sequences of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T as the first genomes of the order Acidiferrobacterales .

Organism information

Classification and features

The cells of Sulfurifustis variabilis skN76T are rod-shaped or filamentous form with varying length, and 0.3–0.5 μm in width (Fig. 1a, Table 1). The cells of Sulfuricaulis limicola HA5T are rod-shaped, 1.2–6.0 μm in length and 0.3–0.5 μm in width (Fig. 1b, Table 1). They are both Gram-stain-negative. Sulfurifustis variabilis and Sulfuricaulis limicola belong to the family Acidiferrobacteraceae within the class Gammaproteobacteria (Fig. 2). They both utilized thiosulfate, tetrathionate and elemental sulfur as electron donors for chemolithoautotrophic growth under aerobic conditions [1, 2].
Fig. 1

Phase-contrast micrographs of Sulfurifustis variabilis skN76T (a) and Sulfuricaulis limicola HA5T (b), grown with thiosulfate at 45 and 28 °C, respectively. Bars, 5 μm

Table 1

Classification and general features of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T according to MIGS recommendations

MIGS ID

Property

Sulfurifustis variabilis skN76T

Sulfuricaulis limicola HA5T

Term

Evidence code a

Term

Evidence code a

 

Classification

Domain Bacteria

TAS [23]

Domain Bacteria

TAS [23]

 

Phylum Proteobacteria

TAS [24]

Phylum Proteobacteria

TAS [24]

 

Class Gammaproteobacteria

TAS [25]

Class Gammaproteobacteria

TAS [25]

 

Order Acidiferrobacterales

TAS [1]

Order Acidiferrobacterales

TAS [1]

 

Family Acidiferrobacteraceae

TAS [1]

Family Acidiferrobacteraceae

TAS [1]

 

Genus Sulfurifustis

TAS [1]

Genus Sulfuricaulis

TAS [2]

 

Species Sulfurifustis variabilis

TAS [1]

Species Sulfuricaulis limicola

TAS [2]

 

Type strain skN76

 

Type strain HA5

 
 

Gram stain

negative

TAS [1]

negative

TAS [2]

 

Cell shape

rod or filaments

TAS [1]

rod

TAS [2]

 

Motility

motile

TAS [1]

not reported

 
 

Sporulation

not reported

 

not reported

 
 

Temperature range

28–46 °C

TAS [1]

8–37 °C

TAS [2]

 

Optimum temperature

42–45 °C

TAS [1]

28–32 °C

TAS [2]

 

pH range; Optimum

6.3–8.9; 6.8–8.2

TAS [1]

6.1–9.2; unknown

TAS [2]

 

Carbon source

bicarbonate

TAS [1]

bicarbonate

TAS [2]

MIGS-6

Habitat

Sediment of a lake

TAS [1]

Sediment of a lake

TAS [2]

MIGS-6.3

Salinity

<2.6 % NaCl (w/v)

TAS [1]

<1.2 % NaCl (w/v)

TAS [2]

MIGS-22

Oxygen requirement

aerobic

TAS [1]

aerobic

TAS [2]

MIGS-15

Biotic relationship

free-living

TAS [1]

free-living

TAS [2]

MIGS-14

Pathogenicity

non-pathogen

NAS

non-pathogen

NAS

MIGS-4

Geographic location

Lake Mizugaki, Japan

TAS [1]

Lake Harutori, Japan

TAS [2]

MIGS-5

Sample collection

November 30, 2010

NAS

April 26, 2012

NAS

MIGS-4.1

Latitude

35°51.5′ N

TAS [26]

42°58.4′ N

NAS

MIGS-4.2

Longitude

138°30.0′ E

TAS [26]

144°23.9′ E

NAS

MIGS-4.4

Altitude

not reported

 

not reported

 

a Evidence codes–IDA Inferred from Direct Assay, TAS Traceable Author Statement (i.e., a direct report exists in the literature), NAS Non-traceable Author Statement (i.e., not directly observed for the living, isolated sample, but based on a generally accepted property for the species, or anecdotal evidence). These evidence codes are from the Gene Ontology project

Fig. 2

Phylogenetic tree showing the relationships of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T with other members of the class Gammaproteobacteria based on 16S rRNA gene sequences aligned by using CLUSTAL W. Desulfatitalea tepidiphila S28bFT was used as an outgroup. This tree was reconstructed using 1412 sites with the neighbor-joining method by using MEGA6 [27]. Percentage values of 1000 bootstrap resamplings are shown at nodes; values below 50 % were not shown

Genome sequencing information

Genome project history

Sulfurifustis variabillis skN76T and Sulfuricaulis limicola HA5T were selected for sequencing as representatives of sulfur-oxidizing bacteria belonging to the order Acidiferrobacterales , to reveal characteristics of their genomes. A summary of the project information is shown in Table 2.
Table 2

Project information

MIGS ID

Property

Sulfurifustis variabilis skN76T

Sulfuricaulis limicola HA5T

Term

Term

MIGS 31

Finishing quality

Completed

Completed

MIGS-28

Libraries used

15–20 kb SMRTbellTM library

10–20 kb SMRTbellTM library

MIGS 29

Sequencing platforms

PacBio RS II

PacBio RS II

MIGS 31.2

Fold coverage

210 ×

142 ×

MIGS 30

Assemblers

RS_HGAP Assembly.2

RS_HGAP Assembly.3

MIGS 32

Gene calling method

Microbial Genome Annotation Pipeline

Microbial Genome Annotation Pipeline

 

Locus Tag

SVA

SCL

 

Genbank ID

AP014936

AP014879

 

GenBank Date of Release

July 29, 2016

July 29, 2016

 

BIOPROJECT

PRJDB4108

PRJDB3927

MIGS 13

Source Material Identifier

DSM 100313

DSM 100373

 

Project relevance

Environmental

Environmental

Growth conditions and genomic DNA preparation

Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T were grown with 20 mM thiosulfate as an energy source in a bicarbonate-buffered medium previously described [1], at 45 and 28 °C, respectively. Genomic DNA samples were prepared by using Wizard® genomic DNA purification kit (Promega, Madison, WI, USA) from approximately 0.2 ml (skN76) or 0.1 ml (HA5) of cell pellets. Amounts of the obtained DNA assessed by spectrophotometry were ca. 270 μg (skN76) and 90 μg (HA5) respectively, and the UV absorption ratio of 260/280 nm was greater than 1.8 in both samples.

Genome sequencing and assembly

The genomic DNA was sheared into approximately 20 kb using g-TUBE (Covaris, Inc., Woburn, MA, USA). The SMRTbellTM templates were prepared from the fragments using SMRTbellTM Template Prep Kit 1.0 (Pacific Biosciences, Menlo Park, CA, USA). The size-selected libraries for sequencing were prepared by using BluePippin (Sage Science, Baverly, MA, USA). The libraries were sequenced on a PacBio RS II instrument (Pacific Biosciences) with P6-C4 chemistry (for Sulfurifustis variabillis skN76T) or P5-C3 chemistry (for Sulfuricaulis limicola HA5T). De novo assembly was performed by using RS_HGAP Assembly.3 (for Sulfurifustis variabillis skN76T) or RS_HGAP Assembly.2 (for Sulfuricaulis limicola HA5T), implemented within the SMRT Analysis v2.3 (Pacific Biosciences) software environment. By assembling 79,017 subreads (837,333,548 bp) of Sulfurifustis variabillis skN76T, two contigs with the lengths of ca. 4.0 Mbp and ca. 5.4 kbp were obtained. The shorter one was identical to a partial sequence of the larger one, and a circular chromosome was manually constructed from the larger contig by finding self-overlapping regions using the in silico Molecular Cloning (R) Genomic Edition (In Silico Biology, Inc., Yokohama, Japan) application. As for Sulfuricaulis limicola HA5T, a single contig (ca. 2.9 Mbp) was obtained by assembling 61,565 subreads (409,124,339 bp), and circular chromosome was manually constructed in the same manner.

Genome annotation

The genomes were annotated automatically using the Microbial Genome Annotation Pipeline [7]. Further manual annotation of the predicted protein-coding sequences was performed on the basis of BLASTP searches against the NCBI nonredundant database. CDSs were annotated as hypothetical protein-coding genes when they met any of the following four criteria in the top hit of the BLASTP analysis: (1) E-value >1e-8, (2) length coverage <60 % against query sequence (3) sequence identity <30 % or (4) function of the hit was unidentified. The WebMGA server was used to assign the genes to Clusters of Ortholog Groups and Protein family domains [811]. The Phobius server was used to predict signal peptides and transmembrane helices [12]. Clustered Regularly Interspaced Short Palindromic Repeat loci were detected using CRISPRfinder [13].

Genome properties

The basic statistics of the genomes are shown in Table 3. Both genomes contained 46 tRNA genes and one rRNA operon. The genome size of Sulfurifustis variabillis skN76T was approximately 1.4 times larger than that of Sulfuricaulis limicola HA5T. CRISPR loci were found only in the genome of Sulfurifustis variabillis skN76T (Table 3). The distribution of genes into COGs functional categories is presented in Table 4.
Table 3

Genome statistics of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T

Attribute

Sulfurifustis variabilis skN76T

Sulfuricaulis limicola HA5T

Value

% of Total

Value

% of Total

Genome size (bp)

3,958,814

100.00

2,864,672

100.00

DNA coding (bp)

3,565,567

90.06

2,567,493

89.63

DNA G + C (bp)

2,670,566

67.46

1,759,557

61.42

DNA scaffolds

1

100.00

1

100.00

Total genes

3913

100.00

2812

100.00

Protein coding genes

3864

98.75

2763

98.26

RNA genes

49

1.25

49

1.74

Pseudo genes

unknown

 

unknown

 

Genes in internal clusters

unknown

 

unknown

 

Genes with function prediction

2930

75.83

2036

73.69

Genes assigned to COGs

2921

75.60

2165

78.36

Genes with Pfam domains

2970

76.86

2208

79.91

Genes with signal peptides

893

23.11

562

20.34

Genes with transmembrane helices

845

21.87

622

22.51

CRISPR repeats

6

 

0

 
Table 4

Number of genes associated with general COG functional categories

Code

Sulfurifustis variabilis skN76T

Sulfuricaulis limicola HA5T

Description

Value

%age

Value

%age

J

164

4.24

159

5.75

Translation, ribosomal structure and biogenesis

A

5

0.13

2

0.07

RNA processing and modification

K

191

4.94

130

4.71

Transcription

L

154

3.99

117

4.23

Replication, recombination and repair

B

1

0.03

1

0.04

Chromatin structure and dynamics

D

36

0.93

31

1.12

Cell cycle control, Cell division, chromosome partitioning

V

43

1.11

29

1.05

Defense mechanisms

T

283

7.32

218

7.89

Signal transduction mechanisms

M

265

6.86

210

7.60

Cell wall/membrane biogenesis

N

66

1.71

64

2.32

Cell motility

U

123

3.18

98

3.55

Intracellular trafficking and secretion

O

185

4.79

142

5.14

Posttranslational modification, protein turnover, chaperones

C

265

6.86

192

6.95

Energy production and conversion

G

148

3.83

101

3.66

Carbohydrate transport and metabolism

E

201

5.20

150

5.43

Amino acid transport and metabolism

F

63

1.63

59

2.14

Nucleotide transport and metabolism

H

167

4.32

129

4.67

Coenzyme transport and metabolism

I

90

2.33

65

2.35

Lipid transport and metabolism

P

189

4.89

127

4.60

Inorganic ion transport and metabolism

Q

56

1.45

35

1.27

Secondary metabolites biosynthesis, transport and catabolism

R

394

10.20

247

8.94

General function prediction only

S

346

8.95

230

8.32

Function unknown

-

943

24.40

598

21.64

Not in COGs

Insights from the genome sequences

In both the genomes of Sulfurifustis variabillis skN76T and Sulfuricaulis limicola HA5T, genes involved in the sulfur oxidation pathway were identified. The genomes of both strains contain genes of the DSR system related to the oxidation of elemental sulfur to sulfite [14, 15]. They contain a dsr gene cluster of identical composition, dsrABEFHCMKLJOPNR (SVA_1954-1967, SCL_1274-1261). There are some dsr genes outside of the gene cluster, dsrAB (SVA_0258-0259, SCL_0256-0257), dsrS (SVA_2921, SCL_0781) and dsrC (SVA_0281, SVA_0284, SVA_0358, SVA_0917, SVA_0969, SVA_1205, SVA_1793, SVA_1949, SVA_2832, SVA_3655; SCL_0275, SCL_0524, SCL_0785, SCL_1279, SCL_1423, SCL_2646).

As genes encoding proteins involved in oxidation of sulfite to sulfate in the cytoplasm, both genomes contain two copies of the aprAB genes encoding an adenosine-5’-phosphosulphate reductase (SVA_2607-2608, SVA_3565-3564; SCL_0600-0601, SCL_2474-2473), along with the sat gene encoding a sulfate adenylyltransferase (SVA_3563, SCL_2472) and the aprM gene (SVA_2609, SCL_0602). In addition, the genome of Sulfuricaulis limicola HA5T contains the hdrAACB genes encoding a Hdr (SCL_2523-2520), but that of Sulfurifustis valiabilis skN76T does not. The AprM and Hdr complex are thought to have similar function that interacts with the adenosine-5’-phosphosulphate reductase [1618]. The genomes also contain the soeABC genes (SVA_2734, SVA_2736-2737; SCL_0523-0521), encoding a membrane-bound polysulfide reductase-like iron-sulfur molybdoprotein, which is suspected to be involved in sulfite oxidation in the cytoplasm [19]. Further, the genome of Sulfurifustis valiabilis skN76T contains the sorAB genes (SVA_1391-1390) related to the direct oxidation of sulfite to sulfate in the periplasm [20].

For thiosulfate oxidation, both genomes contain the soxXYZAB gene cluster (SVA_2999-3003, SCL_2229-2233). Although sulfide oxidation by these bacteria has not been demonstrated, genes related to sulfide oxidation were identified; the fccAB (soxEF) genes encoding a flavocytochrome c/sulfide dehydrogenase (SVA_0067-0066, SVA_3594-3595; SCL_0078-0077) and the sqr gene encoding a sulfide:quinone oxidoreductase (SVA_1781, SVA_2675, SVA3205).

Sulfurifustis variabillis skN76T and Sulfuricaulis limicola HA5T are autotrophic bacteria. They both have two copies of the rbcL and rbcS genes, encoding large and small subunits of ribulose bisphosphate carboxylase/oxygenase (SVA_3460-3459, SVA_3471-3470; SCL_2417-2416, SCL_2425-2424), which is the key enzyme in the Calvin-Benson-Bassham cycle to catalyze inorganic carbon fixation. The two copies of RuBisCO in each genome are phylogenetically distinct, and belong to lineages referred to as green-like form IA and red-like form IC (Fig. 3) [21]. In the form IC RuBisCO coded by rbcL gene (SVA_3460, SCL_2417), Sulfurifustis variabillis skN76T and Sulfuricaulis limicola HA5T have six-amino-acid inserts at the same position where a similar insert was reported from Nitrosospira sp. 40KI [22]. There are two other RuBisCO sequences which have six-amino-acid inserts at the same position, and these sequences with inserts formed a monophyletic cluster in the tree of RuBisCO (Fig. 3). In general, RuBisCO of form IA and IC have different properties which are thought to be advantageous to fix inorganic carbon under different concentrations of carbon dioxide and/or oxygen [21]. Possession of the genes for these two distinct RuBisCO forms may be beneficial to cope with changing environmental conditions, or to thrive in various types of ecosystems.
Fig. 3

Neighbor-joining tree showing the phylogenetic positions of RuBisCO amino acid sequences coded in the genomes of Sulfurifustis variabilis skN76T and Sulfuricaulis limicola HA5T. The sequences aligned by using CLUSTAL W. This tree was reconstructed using 421 sites with MEGA6 [27]. Percentage values of 1000 bootstrap resamplings are shown at nodes; values below 50 % were not shown. The sequences shown in box have six-amino-acid inserts at the same position

Conclusion

This is the first report on complete genome sequences of bacteria belonging to the order Acidiferrobacterales . The genome analysis of Sulfurifustis variabillis skN76T and Sulfuricaulis limicola HA5T revealed that they have similar sets of genes involved in sulfur oxidation pathways. In the both genomes, redundancies of the genes for sulfur oxidation and inorganic carbon fixation were observed, as represented by multiple copies of dsrAB, aprAB and rbcLS. Such redundancies may provide physiological flexibility to the chemolithotrophic sulfur oxidizers which are fully depending on these functions to obtain energy and carbon source for growth.

Abbreviations

MiGAP: 

Microbial Genome Annotation Pipeline

Hdr: 

Heterodisulfide reductase

DSR: 

Dissimilatory sulfite reductase

Declarations

Acknowledgements

This study was supported by JSPS KAKENHI Grant Number 15 K07209 to H. Kojima. We thank R. Tokizawa and A. Shinohara for their technical assistance.

Authors’ contribution

MF and HK designed the study. HK characterized the strains and prepared genomic DNA. KU, TW and AM performed the bioinformatics analysis. KU and HK wrote the draft of manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
The Institute of Low Temperature Science, Hokkaido University

References

  1. Kojima H, Shinohara A, Fukui M. Sulfurifustis variabilis gen. nov., sp. nov., a sulfur oxidizer isolated from a lake, and proposal of Acidiferrobacteraceae fam. nov. and Acidiferrobacterales ord. nov. Int J Syst Evol Microbiol. 2015;65:3709–13.View ArticlePubMedGoogle Scholar
  2. Kojima H, Watanabe T, Fukui M. Sulfuricaulis limicola gen. nov., sp. nov., a sulfur oxidizer isolated from a lake. Int J Syst Evol Microbiol. 2016;66:266–70.View ArticlePubMedGoogle Scholar
  3. Hallberg KB, Hedrich S, Johnson DB. Acidiferrobacter thiooxydans, gen. nov. sp. nov.; an acidophilic, thermo-tolerant, facultatively anaerobic iron- and sulfur-oxidizer of the family Ectothiorhodospiraceae. Extremophiles. 2011;15:271–9.View ArticlePubMedGoogle Scholar
  4. Kelly DP, Wood AP. Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen. nov., Halothiobacillus gen. nov. and Thermithiobacillus gen. nov. Int J Syst Evol Microbiol. 2000;50:511–6.View ArticlePubMedGoogle Scholar
  5. Williams KP, Kelly DP. Proposal for a new class within the phylum Proteobacteria, Acidithiobacillia classis nov., with the type order Acidithiobacillales, and emended description of the class Gammaproteobacteria. Int J Syst Evol Microbiol. 2013;63:2901–6.View ArticlePubMedGoogle Scholar
  6. Dyksma S, Bischof K, Fuchs BM, Hoffmann K, Meier D, Meyerdierks A, et al. Ubiquitous Gammaproteobacteria dominate dark carbon fixation in coastal sediments. ISME J. 2016;10(8):1–15.View ArticleGoogle Scholar
  7. Sugawara H, Ohyama A, Mori H, Kurokawa K. Microbial Genome Annotation Pipeline (MiGAP) for diverse users. The 20th International Conference on Genome Informatics (GIW2009) Poster and Software Demonstrations (Yokohama). 2009;S001-1-2.Google Scholar
  8. Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011;12:444.View ArticlePubMedPubMed CentralGoogle Scholar
  9. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10.View ArticlePubMedGoogle Scholar
  10. Eddy SR. Profile hidden Markov models. Bioinformatics. 1998;14:755–63.View ArticlePubMedGoogle Scholar
  11. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, et al. The Pfam protein families database. Nucleic Acids Res. 2010;38:D211–22.View ArticlePubMedGoogle Scholar
  12. Kall L, Krogh A, Sonnhammer ELL. Advantages of combined transmembrane topology and signal peptide prediction-the Phobius web server. Nucleic Acids Res. 2007;35:W429–32.View ArticlePubMedPubMed CentralGoogle Scholar
  13. Grissa I, Vergnaud G, Pourcel C. CRISPRFinder: a web tool to identify clustered regularly interspaced short palindromic repeats. Nucleic Acids Res. 2007;35:W52–7.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Pott AS, Dahl C. Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology. 1998;144:1881–94.View ArticlePubMedGoogle Scholar
  15. Dahl C, Engels S, Pott-Sperling AS, Schulte A, Sander J, Lübbe Y, et al. Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum. J Bacteriol. 2005;187:1392–404.View ArticlePubMedPubMed CentralGoogle Scholar
  16. Parey K, Demmer U, Warkentin E, Wynen A, Ermler U, Dahl C. Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum. PLoS One. 2013;8:e7407.View ArticleGoogle Scholar
  17. Pires RH, Lourenço AI, Morais F, Teixeira M, Xavier AV, Saraiva LM, et al. A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774. Biochim Biophys Acta. 2003;1605:67–82.View ArticlePubMedGoogle Scholar
  18. Meyer B, Kuever J. Molecular analysis of the distribution and phylogeny of dissimilatory adenosine-5’-phosphosulfate reductase-encoding genes (aprBA) among sulfur-oxidizing prokaryotes. Microbiology. 2007;153:3478–98.View ArticlePubMedGoogle Scholar
  19. Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R. Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process. Microbiology. 2013;159:2626–38.View ArticlePubMedGoogle Scholar
  20. Kappler U, Bennett B, Rethmeier J, Schwarz G, Deutzmann R, McEwan AG, et al. Sulfite:cytochrome c oxidoreductase from Thiobacillus novellus — purification, characterization and molecular biology of a heterodimeric member of the sulfite oxidase family. J Biol Chem. 2000;275:13202–12.View ArticlePubMedGoogle Scholar
  21. Badger MR, Bek EJ. Multiple Rubisco forms in proteobacteria: their functional significance in relation to CO2 acquisition by the CBB cycle. J Exp Bot. 2008;59:1525–41.View ArticlePubMedGoogle Scholar
  22. Utåker JB, Andersen K, Aakra Å, Moen B, Nes IF. Phylogeny and functional expression of ribulose 1,5-Bisphosphate carboxylase/oxygenase from the autotrophic ammonia-oxidizing bacterium Nitrosospira sp. Isolate 40KI. J Bacteriol. 2002;184:468–78.View ArticlePubMedPubMed CentralGoogle Scholar
  23. Woese CR, Kandler O, Wheelis ML. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci U S A. 1990;87:4576–9.View ArticlePubMedPubMed CentralGoogle Scholar
  24. Garrity GM, Bell JA, Lilburn T. Phylum XIV. Proteobacteria phyl. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, Volume 2, Part B. 2nd ed. New York: Springer; 2005. p. 1.Google Scholar
  25. Garrity GM, Bell JA, Lilburn T. Class III. Gammaproteobacteria class. nov. In: Garrity GM, Brenner DJ, Krieg NR, Staley JT, editors. Bergey’s Manual of Systematic Bacteriology, Volume 2, Part B. 2nd ed. New York: Springer; 2005. p. 1.Google Scholar
  26. Kojima H, Iwata T, Fukui M. DNA-based analysis of planktonic methanotrophs in a stratified lake. Freshw Biol. 2009;54:1501–9.View ArticleGoogle Scholar
  27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.View ArticlePubMedPubMed CentralGoogle Scholar

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