Open Access

Complete genome of Nitrosospira briensis C-128, an ammonia-oxidizing bacterium from agricultural soil

  • Marlen C. Rice1,
  • Jeanette M. Norton1Email author,
  • Frederica Valois2,
  • Annette Bollmann3,
  • Peter J. Bottomley4,
  • Martin G. Klotz5, 6,
  • Hendrikus J. Laanbroek7, 8,
  • Yuichi Suwa9,
  • Lisa Y. Stein10,
  • Luis Sayavedra-Soto4,
  • Tanja Woyke11,
  • Nicole Shapiro11,
  • Lynne A. Goodwin12,
  • Marcel Huntemann11,
  • Alicia Clum11,
  • Manoj Pillay11,
  • Nikos Kyrpides11,
  • Neha Varghese11,
  • Natalia Mikhailova11,
  • Victor Markowitz11,
  • Krishna Palaniappan11,
  • Natalia Ivanova11,
  • Dimitrios Stamatis11,
  • T. B. K. Reddy11,
  • Chew Yee Ngan11 and
  • Chris Daum11
Standards in Genomic Sciences201611:46

https://doi.org/10.1186/s40793-016-0168-4

Received: 10 December 2015

Accepted: 18 July 2016

Published: 28 July 2016

Abstract

Nitrosospira briensis C-128 is an ammonia-oxidizing bacterium isolated from an acid agricultural soil. N. briensis C-128 was sequenced with PacBio RS technologies at the DOE-Joint Genome Institute through their Community Science Program (2010). The high-quality finished genome contains one chromosome of 3.21 Mb and no plasmids. We identified 3073 gene models, 3018 of which are protein coding. The two-way average nucleotide identity between the chromosomes of Nitrosospira multiformis ATCC 25196 and Nitrosospira briensis C-128 was found to be 77.2 %. Multiple copies of modules encoding chemolithotrophic metabolism were identified in their genomic context. The gene inventory supports chemolithotrophic metabolism with implications for function in soil environments.

Keywords

Nitrosospira Ammonia-oxidizing bacteriaNitrificationAgricultural soilAmmonia monooxygenaseNitrous oxideChemolithotroph

Introduction

The first step in the aerobic nitrification process is the oxidation of ammonia to nitrite, mediated mainly by AOB or AOA in soil environments. The most numerous AOB isolated or detected by non-cultural methods in aerobic agricultural surface soils are consistently members of the Nitrosospira genus [1]. Nitrosospira briensis C-128 [2] is a chemolithoautotrophic ammonia-oxidizing betaproteobacterium (order Nitrosomonadales , family Nitrosomonadaceae , genus Nitrosospira [39]) isolated from a fertilized soil under cultivation for blueberry in Falmouth, Massachusetts, USA in 1971. The genome of Nitrosospira briensis C-128 is the third genome sequence from the genus Nitrosospira [810] to be published [1113] and thus provides an important comparison among Nitrosospira . This report includes a summary of the genome sequence and selected features for Nitrosospira briensis C-128 and results are publically available in GenBank accession CP012371.

Organism information

Classification and features

Nitrosospira briensis was described by Winogradsky and & Winogradsky in 1933 [8] as an ammonia-oxidizing bacterium isolated from soil. The genus name, Nitrosospira , is derived from two Latin roots: nitrosus, meaning nitrous, and spira, indicating spiral. The species name briensis, refers to the original isolation location near Brie, France. The culture described by Winogradsky & Winogradsky [8] was not maintained and reisolation of a replacement strain was reported by Watson in 1971 [14]. At approximately the same time, N. briensis strain C-128 was isolated by enrichment culturing [15] from a surface soil sample (pH 6.2) collected from a fertilized blueberry patch in East Falmouth, Massachusetts in 1971 (Frederica Valois). In 1993, the genus Nitrosospira was emended to include the former genera of Nitrosovibrio and Nitrosolobus [9] based on the high identities of the 16S rRNA gene sequences. Nitrosospira briensis was designated the type species for the genus with strain C-76 as the type strain (also known as strain Nsp10 [16]1). The full-length 16S rRNA gene sequence of N. briensis C-128 is 99 % identical to the N. briensis strain C-76/Nsp10 sequence (Fig. 1). The culture of N. briensis strain C-128 was received in the Norton laboratory from F. Valois (Woods Hole Oceanographic Institution) in 1995. Nitrosospira briensis C-128 is presently maintained in a culture collection at WHOI and may be obtained upon request from J.M. Norton. Classification and general features of Nitrosospira briensis C-128 are provided as Minimum Information about the Genome Sequence (MIGS) in Table 1. Electron micrographs of the pure culture organism are shown in Fig. 2 revealing the tight spirals visible with TEM negative staining and the convoluted surface of this Nitrosospira as revealed by SEM.
Fig. 1

The phylogenetic tree highlighting the position of Nitrosospira briensis C-128 relative to other Nitrosomonadaceae [48] and Spirillum volutans (outgroup). The tree was inferred from 1417 aligned characters of the 16S rRNA gene sequence by the neighbour-joining method [49] using the sotware MEGA [50]. Support values (%) at branch points are from 1000 NJ bootstrap replicates and shown only for values exceeding 60 %. GenBank references are for genomes (full-length 16S rRNA gene extracted) or are the near full-length 16S rRNA sequences [51]. Bold denotes a genome sequence available (NCBI or GOLD), whereas bold blue denotes the published genomes: Nitrosomonas europaea [52], “Nitrosomonas eutropha” [53], “Nitrosomonas communis” [54], Nitrosomonas sp. AL212 [55], “Nitrosomonas ureae” [56], Nitrosomonas sp. Is79A3 [57], Nitrosospira briensis C-128 (this study), Nitrosospira lacus APG3 [11] and Nitrosospira multiformis [12]

Table 1

Classification and general features of Nitrosospira briensis C-128 [42, 43]

MIGS ID

Property

Term

Evidence codea

 

Current classification

Domain Bacteria

TAS [44]

 

Phylum Proteobacteria

TAS [45]

 

Class Betaproteobacteria

TAS [7, 46]

 

Order Nitrosomonadales

TAS [5, 46]

 

Family Nitrosomonadaceae

TAS [4, 46]

 

Genus Nitrosospira

TAS [6, 8]

 

Species Nitrosospira briensis

TAS [6, 8]

 

Strain C-128

IDA

 

Gram stain

negative

TAS [14]

 

Cell shape

Spiral/vibrioid

IDA

 

Motility

motile

TAS [14]

 

Sporulation

Non-sporulating

TAS [14]

 

Temperature range

15–30 °C

TAS [14]

 

Optimum temperature

25–28 °C

TAS [14]

 

pH range; Optimum

6.0–8.2;7.0

TAS [14]

 

Carbon source

carbon dioxide; carbonate

TAS [14]

 

Energy source

ammonia oxidation

TAS [14]

 

Energy metabolism

chemolithotroph

TAS [14]

MIGS-6

Habitat

soil (acid)

IDA

MIGS-6.3

Salinity

Non-halophile

TAS [14]

MIGS-22

Oxygen requirement

Aerobic

TAS [14]

MIGS-23

Isolation and growth conditions

Isolation after enrichment on inorganic ammonium salts medium

TAS [14]

MIGS-15

Biotic relationship

Free living

NAS

MIGS-14

Pathogenicity

Non-pathogen

NAS

 

Biosafety level

1

NAS

MIGS-4

Geographic location

East Falmouth, MA, USA

NAS

MIGS-4.1

Latitude

41°35′38″ N

NAS

MIGS-4.2

Longitude

70°34′20″ W

NAS

MIGS-4.3

Depth

surface soil

NAS

MIGS-4.4

Altitude

6 m

NAS

MIGS-5

Sample collection

1971 Feb 18

NAS

aEvidence codes – IDA Inferred from Direct Assay (first time in publication), TAS Traceable Author Statement (i.e. a direct report exists in the literature), NAS Non-traceable Author Statement (i.e. not directly observed for 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 [47]

Fig. 2

Electron micrographs of N. briensis. A) TEM prepared by negative staining as previously described [14, 15]. Scale is 1000 nm. B) SEM of Nitrosospira briensis C-128. Glass coverslips were placed in a growing culture for approximately one month, removed and then fixed with 2 % glutaraldehyde in 0.1 % HEPES buffer overnight. The samples were subjected to alcohol series dehydration (50-100 % ethanol) and then chemically dried using hexamethyldisilazane. The image shows presumptive invaginations of the membranes of the cell. Scale is 500 nm

Genome sequencing information

Genome project history

Nitrosospira briensis C-128 was chosen for sequencing through the Community Science Program (2010) of the DOE Joint Genome Institute as an important representative of the AOB to improve the scope and quality of intra- and inter-generic comparisons in the Nitrosomonadales . The chemolithotrophic metabolism of the AOB, the pathways for production of nitrous oxide and urea metabolism were additional motivating interests in sequencing this genome. Sequencing, finishing, and annotation were accomplished by JGI. The genome sequence has been deposited in the Genome OnLine Database [17] and is part of the NCBI Reference Sequence Collection [18]. A summary of the project information is found in Table 2.
Table 2

Genome sequencing project information

MIGS ID

Property

Term

MIGS 31

Finishing quality

Finished

MIGS-28

Libraries used

One library, PacBio SMRTbell Library

MIGS 29

Sequencing platforms

PacBio RS

MIGS 31.2

Fold coverage

176X

MIGS 30

Assemblers

HGAP v. 2.2.0.p1 [23]

MIGS 32

Gene calling method

Prodigal, GenePRIMP

 

Locus Tag

F822

 

Genbank ID

CP012371.1

 

GenBank Release Date

14-Aug-2015

 

GOLD ID

Gp0006506

 

BioProject ID

PRNJA183056

MIGS 13

Source Material Identifier

Nitrosospira briensis C-128 WHOI

Project relevance

Environmental, Biogeochemical cycling of nitrogen, Biotechnological

Growth conditions and genomic DNA preparation

Nitrosospira briensis C-128 was grown in a 25 mM ammonium medium pH 7 containing mineral salts and phenol red at 28 °C in 100 ml of media in 500 ml flasks as described previously [19]. The pH was adjusted to neutral using 0.5 M KHCO3 as needed during growth. Early stationary phase cultures were checked at harvest for heterotrophic contamination by plating 0.1 mL on ¼ strength nutrient agar plates and incubating for two weeks. Cells were harvested from four 100 mL cultures by centrifugation (13,000 RCF for 30 min). Bacterial genomic DNA (gDNA) was isolated using the CTAB protocol recommended by JGI [20]. Size and quality of the gDNA was assessed via gel electrophoresis and amplification of the V4 region of the 16S rRNA gene using universal primers [21] followed by sequencing at the Center for Integrative Biosystems, USU on the ABI PRISM™ 3730 DNA Analyzer using BigDye terminator chemistry. The gDNA was of the expected size (greater than 23 kbp) and no contaminating organisms were detected by partial 16S rRNA gene sequencing of 10 replicate reactions or by plating. Approximately 20 μg of DNA was submitted to JGI for sequencing.

Genome sequencing and assembly

The genomic DNA of Nitrosospira briensis C-128 was sequenced at the DOE JGI using the Pacific Biosciences (PacBio) sequencing technology [22]. All general aspects of sample handling, library construction and sequencing followed JGI isolate sequencing protocols. A PacBio SMRTbell™ library was constructed and sequenced on the PacBio RS platform, which generated 148,206 reads totaling 519.8Mbp. Raw reads were assembled using HGAP v. 2.2.0.p1 [23]. The final draft assembly contained one contig in one scaffold, totaling 3.2 Mbp in size. The input read coverage was 176.1×. An earlier version of the genome was sequenced using the Illumina Hi-Seq 2000 platform. However, this earlier sequence assembly JHVX00000000.1 remained in 31 scaffolds (sequences JHVX01000001.1-JHVX01000031.1) with the nearly identical repeats of several key catabolic gene clusters remaining unresolved. Previously, genome closure for Nitrosospira [12] was achieved only after extensive directed finishing to correctly assemble long nearly identical repeats of gene clusters encoding key catabolic modules including ammonia monooxygenase (amo) for the activation of substrate and hydroxylamine dehydrogense (haoA) and heme-cytochrome c proteins (cycAB) for the extraction of electrons and their delivery to the quinone pool in the membrane [24]. The long read capability of the PacBio platform and our depth of coverage enabled sufficient discrimination of repeats to assemble across multiple nearly identical regions into a single contig representing the chromosome of the bacterium. For predicted genes outside of gaps and repeat regions the PacBio and the Illumina predicted genes were 100 % identical. Therefore, we did not combine the Illumina Hi-Seq data with the PacBio data for the complete genome sequence CP012371 reported here.

Genome annotation

Genes were identified using Prodigal [25], as part of the JGI’s Microbial annotation pipeline followed by a round of manual curation using GenePRIMP [26]. The predicted CDSs were translated and used to search the NCBI nonredundant database, UniProt, TIGRFam, Pfam, KEGG, COG, and InterPro databases. Transfer RNA genes were identified using the tRNAScanSE tool [27]. Ribosomal RNA genes were found by searches against models of the ribososmal RNA genes built from SILVA [28]. Other non-coding RNAs were found using INFERNAL [29]. Further gene prediction and manual curation was performed within the Integrated Microbial Genomes (IMG) platform [30] developed at JGI.

Genome properties

The genome of Nitrosospira briensis C-128 contains 3,210,113-bp in one chromosome with a GC content of 53.25 % and no plasmids (Fig. 3). The genome contains one complete ribosomal RNA operon similar to other AOB [3]. Coding bases (2,758,471) comprised 85.93 % of the total. We identified 3018 protein encoding genes, 55 RNA genes and 130 pseudogenes. For the identified genes, 74.23 % had a function prediction associated with them. The two-way average nucleotide identity [31] between the chromosomes of Nitrosospira multiformis ATCC 25196 [9, 32, 33] and Nitrosospira briensis C-128 was found to be 77.2 % confirming species delineation [34]. The genome statistics are summarized in Table 3 and genes associated with COG functional categories are summarized in Table 4.
Fig. 3

a Graphical map of the genome. From the outside to the center: genes on forward stand and Genes on reverse strand (color by COG categories see legend), RNA genes (tRNAs green, rRNAs red, other RNAs black), GC content, GC skew. b Legend for COG category colors

Table 3

Genome statistics

Attribute

Value

% of Total

Genome size (bp)

3,210,113

100.00

DNA coding (bp)

2,758,471

85.93

DNA G + C (bp)

1,709,486

53.25

DNA scaffolds

1

100.00

Total genes

3073

100.00

Protein coding genes

3018

98.2

RNA genes

55

1.79

Pseudo genes

130

4.23

Genes with internal clusters

394

12.82

Genes with function prediction

2232

72.63

Genes assigned to COGs

1849

60.17

Genes with Pfam domains

2303

74.94

Genes with signal peptides

290

9.44

Genes with transmembrane helices

741

24.11

CRISPR repeats

1

0.02

Table 4

Number of genes associated with general COG functional categories

Code

Value

%age

Description

J

149

7.32

Translation, ribosomal structure and biogenesis

A

1

0.05

RNA processing and modification

K

82

4.03

Transcription

L

122

6.00

Replication, recombination and repair

B

1

0.05

Chromatin structure and dynamics

D

25

1.23

Cell cycle control, Cell division, chromosome partitioning

V

24

1.18

Defense mechanisms

T

75

3.69

Signal transduction mechanisms

M

167

8.21

Cell wall/membrane biogenesis

N

53

2.60

Cell motility

U

67

3.29

Intracellular trafficking and secretion

O

114

5.60

Posttranslational modification, protein turnover, chaperones

C

153

7.52

Energy production and conversion

G

88

4.32

Carbohydrate transport and metabolism

E

140

6.88

Amino acid transport and metabolism

F

54

2.65

Nucleotide transport and metabolism

H

99

4.86

Coenzyme transport and metabolism

I

73

3.59

Lipid transport and metabolism

P

106

5.21

Inorganic ion transport and metabolism

Q

57

2.80

Secondary metabolites biosynthesis, transport and catabolism

R

202

9.93

General function prediction only

S

183

8.99

Function unknown

-

1224

39.83

Not in COGs

Insights from the genome sequence

Selected functional inventory in the complete genome sequence

Nitrosospira briensis C-128 contains complete “amo” and “hao” gene clusters in three nearly identical copies on the chromosome. The full-length amoCABEDcopCD gene cluster is repeated twice (F822_1680-1686, & 2228–2234) while the third cluster contains only the three structural “amo” genes, amoCAB (F822_0880-0878). As in most other betaproteobacterial AOB genomes, the N. briensis C-128 genome contains three additional amoC singleton genes (F822_0485, 1530, & 2742). The “hydroxylamine-ubiquinone redox module” (HURM) [24] is encoded by the haoAB-cycAB gene cluster, which occurs three times (F822_0640-0643, 0873–0876, 1808–1811) in the genome sequence. The N. briensis C-128 genome also encodes nitrosocyanin (ncyA; F822_2886), a protein unique to ammonia-oxidizing bacteria, which possibly functions in the regulation of electron transfer [35]. A urease operon containing α, β, & γ subunit-encoding genes as well as genes encoding accessory proteins E, F, G, & H (F822_0450-0456) is preceded by a urea transporter gene (utp; F822_0449). Genes encoding alternative catabolic inventory such as hydrogenase were not identified. The N. briensis C-128 genome contains a single gene cluster encoding the Calvin-Benson-Bassham cycle for carbon assimilation including the carboxylation reaction, which is encoded by a single-copy cbb operon in the Form 1C (red-like) subgroup (F822_1009-1012) with > 90 % identity with homologous genes in Nitrosospira multiformis [36] and Nitrosospira sp. 40KI [37].

Genes encoding inventory implicated in nitrogen oxide metabolism and /or nitrosative stress [38] include those for copper nitrite reductase (nirK, singleton F822_2604) and a possible quinol nitric oxide reductase (qNOR) encoding gene (F822_0115). Similar to arrangements in many AOB genomes, a gene cluster (norSY-senC-orf1) (F822_ 1803–1806) encoding nitric oxide reductase heme-copper oxidase (sNOR) was found upstream of a nitrite transporter gene (F822_1807) and one of the three haoAB-cycAB clusters. However, the norCBQD cluster encoding cytochrome C nitric oxide reductase (cNOR) was not found. The genes encoding precursors of cytochromes c’-beta (cytS) and P-460 (cytL) were not detected in the C-128 genome sequence. The gene of NO-responsive regulator (nnrS) was present albeit truncated.

CRISPR/Cas System Nitrosospira briensis C-128 contains a CRISPR/Cas system located at F822_1846-1851 suggestive of phage interactions [39]. The CRISPR-associated (CAS) proteins belong to the subtype 1-F ( Yersinia pestis type) [40]. The CRISPR contains 11 spacers each with 32 bp. No matches between these spacers and protospacers in viral genomes were detected in the NCBI non-redundant database. The direct repeat sequence in the CRISPR is 28 bp: TTTCTGAGCTGCCTATGCGGCAGTGAAC. As soil viral metagenomes become better characterized, associations between viral protospacers and the spacers found in N. briensis CRISPR may help to identify possible phage types of N. briensis .

Conclusions

Nitrosospira briensis C-128 has a suite of genes enabling it to survive in soil environments as a chemolithoautotroph. The completion of several genomes in the Nitrosospira genus will facilitate a comprehensive analysis of the genetic toolkit that enables these AOB to co-inhabit the terrestrial niche. Further experiments elucidating gene function, especially those involved in the metabolism of nitrogen oxides and related to nitrosative stress [41], will increase the relevance of the completed genome of Nitrosospira briensis C-128. The evolutionary relationships in the genera of the Nitrosomonadaceae are currently under reconsideration.

Footnotes
1

Editor’s note – Readers are advised that the published record regarding the type strain and a proposed neotype strain of Nitrosospira briensis is problematic. Although the Approved Lists of Bacterial Names (Int J Syst Bacteriol 1980; 30:225) list the type as “no culture available”, Koops and Harms subsequently published on strain Nsp 10 as the equivalent to ATCC 25971 (Arch Microbiol 1985; 141:214–218)

 

Abbreviations

AOA: 

Ammonia-oxidizing archaea

AOB: 

Ammonia-oxidizing bacteria

WHOI: 

Woods Hole Oceanographic Institution

Declarations

Acknowledgements

We thank Frederica Valois for years of maintenance and documentation of the Stanley Watson and John Waterbury collection of AOB at WHOI and for sending us this organism. Original TEM micrographs were obtained from the WHOI Archives by F. Valois. We would like to thank Fen-Ann Shen (USU) for her help in obtaining the SEM. We thank JGI for re-sequencing this genome using improved sequencing technologies. The work was supported by the U.S. Department of Energy, Office of Science JGI under Contract No. DE-AC02-05CH11231 for CSP 2010 project 1012224; USDA NIFA Award 2011-67019-30178, and the Utah Agricultural Experiment Station, Utah State University project UTA00371 and approved as journal paper 8806.

Authors’ contributions

MCR isolated the DNA, worked on directed sequencing, obtained the SEM and wrote the first draft of the article; FV maintains AOB culture collection at WHOI and provided the strain and original TEM, JMN was the PI of the original CSP and lab director; sequencing, assembly and annotation at JGI, project manager at JGI was NS. JMN drafted the manuscript, which was subsequently discussed, revised and improved by all co-authors. 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)
Utah State University
(2)
Woods Hole Oceanographic Institution
(3)
Miami University
(4)
Oregon State University
(5)
Queens College in The City University of New York
(6)
The Institute of Marine Microbes and Ecospheres, Xiamen University
(7)
Netherlands Institute of Ecology
(8)
Utrecht University
(9)
Chuo University
(10)
University of Alberta
(11)
DOE Joint Genome Institute
(12)
Los Alamos National Laboratory, Bioscience Division

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