Open Access

Draft genome of Prochlorothrix hollandica CCAP 1490/1T (CALU1027), the chlorophyll a/b-containing filamentous cyanobacterium

Standards in Genomic Sciences201611:82

https://doi.org/10.1186/s40793-016-0204-4

Received: 24 November 2015

Accepted: 11 October 2016

Published: 18 October 2016

Abstract

Prochlorothrix hollandica is filamentous non-heterocystous cyanobacterium which possesses the chlorophyll a/b light-harvesting complexes. Despite the growing interest in unusual green-pigmented cyanobacteria (prochlorophytes) to date only a few sequenced genome from prochlorophytes genera have been reported. This study sequenced the genome of Prochlorothrix hollandica CCAP 1490/1T (CALU1027). The produced draft genome assembly (5.5 Mb) contains 3737 protein-coding genes and 114 RNA genes.

Keywords

CyanobacteriaProchlorophytes Prochlorothrix hollandica Comparative genomics

Introduction

The majority of cyanobacteria use chl a as a sole magnesium tetrapyrrole and common phycobilisome functioning as the bulk LHC. The prochlorophytes are a unique pigment subgroup of phylum Cyanobacteria – besides chl a, they contain other chls (b; 2,4-divinyl a; 2,4-divinyl b; f; g) as antennal pigments and simultaneously do not depend on the PBP-containing photoreceptors [1]. Prochlorophytes demonstrating these outgroup features are few and encompass three marine unicellular genera ( Prochloron , Prochlorococcus , Acaryochloris) and one freshwater filamentous ( Prochlorothrix ). Unicellular Prochlorococcus spp. dominate in phytoplankton of oligotrophic regions of the world’s ocean and they are of exceptional importance from the viewpoint of global primary productivity [2]. Prochloron sp. and Acaryochloris sp. were isolated in symbiotic association with colonial ascidians [3, 4]. In contrast to other prochlorophytes distribution, P. hollandica is characterized by low abundance and patchy distribution [5]; more detailed genome analysis would explain the ecophysiological background of this microorganism.

The genus Prochlorothrix is represented by two cultivable free-living species: Prochlorothrix hollandica and Prochlorothrix scandica, as well as a number of unculturable strains, originating from environmental 16S rRNA sequences [6]. The distinction between P. hollandica and P. scandica is predominantly based on the molecular-genetic characters: DNA reassociation less than 30 % and DNA GC mol% content difference more than 5 % [5].

P. hollandica was isolated from the water bloom of Loosdrecht lake (near Amsterdam, Nertherlands) and validly published under the rules of Bacteriological Code as the type strain CCAP 1490/1T [7, 8]. The strain CCAP 1490/1 was generously supplied in 1994 by Dr. Hans C.P. Matthijs (Amsterdam University) and since then stored as CALU1027 at the Collection of Cultures of Algae and Microorganisms of St. Petersburg State University, CALU [9]. Prochlorothrix hollandica is also maintained as different strains under collection indexes CCMP34, CCMP682, NIVA-5/89, SAG10.89, and the strain PCC9006 was reported as well [10]. Another filamentous strain Prochlorothrix scandica was isolated from the phytoplankton of Lake Mälaren (Sweden), and is maintained as NIVA-8/90 and CALU1205 [11].

Among prochlorophytes at first were sequenced small genomes of unicellular Prochlorococcus sp. strains from LL- and HL-clades [2, 12, 13]. Four sequenced genomes of symbiotic Prochloron didemni P1-P4 are second in number [14]. Acaryochloris marina genomes were sequenced in the strains CCME5410 and MBIC11017 [15], but only one paper mentioned about P. hollandica PCC9006 genome sequenced by Shich et al. in the context of improving of global cyanobacterial phylogeny [16]. Here we report that genomic DNA of P. hollandica CCAP 1490/1T (CALU1027) was sequenced and obtained draft genome was annotated in order to conduct investigations in the field of comparative genomics of cyanobacteria and prochlorophytes.

Organism information

Classification and features

A representative genomic 16S rDNA sequence of strain P. hollandica CCAP 1490/1T (CALU1027) was compared with another prochlorophytes and also with cyanobacterial type strains sequences obtained from GenBank. The tree was reconstructed using neighbor-joining with the Kimura-2 parameter substitution model in MEGA 6.0 [17, 18]. The phylogenetic position of P. hollandica CALU1027 represents in Fig. 1. Representatives of the genus Prochlorothrix are morphologically similar to other filamentous non-heterocystous cyanobacteria (Subsection III, Oscillatoriales) [19]. In particular, P. hollandica CALU1027 produces long (>300 μm) straight, unbranched, non-motile trichomes (Fig. 2). Individual cells are 1.6 ± 0.1 μm wide and 11.8 ± 0.9 μm long that matches with the data reported [2, 4]. The opaque polar aggregates of gas vesicles resemble of those presented in Pseudanabaena type, but P. hollandica trichomes possess more slight intercellular constrictions (1/5 − 1/8 cell diameter). Trichomes multiply by means of occasional breakage without the resulting formation of hormogonia. Light- or electron microscopic-visible sheath and mucilaginous capsule were never observed; cell envelope demonstrates a typical Gram-negative triple-layer contour [5]. A brief survey of P. hollandica CALU1027 properties according to MIGS recommendations [20] is given in Table 1.
Fig. 1

Phylogenetic position of P. hollandica CALU1027 within cyanobacteria. GenBank accession numbers are indicated in parentheses. The numbers above branches indicate bootstrap support from 1000 replicates

Fig. 2

Light micrograph of P. hollandica CALU1027. Scale bar 10 μm

Table 1

Classification and general features of P. hollandica CALU1027

MIGS ID

Property

Term

Evidence codea

 

Current classification

Domain Bacteria

TAS [33]

 

Phylum BX Cyanobacteria

TAS [19]

 

Class Photobacteria

TAS [34]

 

Order Prochlorales

TAS [34]

 

Family Prochlorothrichaceae

TAS [8]

 

Genus Prochlorothrix

TAS [8]

 

Species Prochlorothrix hollandica

TAS [8]

 

Type strain CCAP 1490/1T

TAS [8]

 

Gram stain

Not reported

 
 

Cell shape

Elongated rods

TAS [5, 8]

 

Motility

Nonmotile

TAS [8]

 

Sporulation

Not reported

 
 

Temperature range

15 °C − 30 °C

TAS [8]

 

Optimum temperature

20 °C

TAS [5, 8]

 

pH range, Optimum

8.4

TAS [8]

 

Carbon source

Autotroph

TAS [8]

 

Energy source

Phototroph

TAS [8]

MIGS-6

Habitat

Freshwater

TAS [8]

MIGS-6.3

Salinity

Less than 25 mM

TAS [5, 8]

MIGS-22

Oxygen requirement

Aerobic

TAS [8]

MIGS-6.4

Chlorophyll type

Chlorophylls a and b

TAS [8]

MIGS-15

Biotic relationships

Free-living

TAS [8]

MIGS-14

Pathogenicity

Not reported

 

MIGS-4

Geographic location

Loosdrecht lake, The Netherlands

TAS [8]

MIGS-5

Sample collection time

9 July, 1984

TAS [8]

MIGS-4.1

Latitude

52.20 N

TAS [8]

MIGS-4.2

Longitude

5.5 E

TAS [8]

MIGS-4.3

Depth

0.2 m

TAS [8]

MIGS-4.4

Altitude

2 m

NAS

aEvidence codes - 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 [25]

Genome sequencing information

Genome project history

The WGS project AJTX02 has been deposited at DDBJ/EMBL/GenBank under accession AJTX00000000 (20.02.2013) and updated, in this research, as Draft Genome Project AJTX00000000.2 (29.04.2015). The assembled contigs have been deposited in NCBI. The project information and its association with the MIGS are summarized in Table 2.
Table 2

Project information

MIGS ID

Property

Term

MIGS-31

Finishing quality

Draft

MIGS-28

Libraries used

Illumina paired-end library

MIGS-29

Sequencing platform

Illumina MiSeq

MIGS-31.2

Fold coverage

30×

MIGS-30

Assemblers

SPAdes v. 3.5.0

MIGS-32

Gene calling method

GeneMarkS+

Locus Tag

PROH

GenBank ID

GCA_000341585.2

Genbank date of release

20 February, 2013

Gold ID

Gp0010359

BioProject

PRJNA63021

DDBJ ID

AJTX00000000.2

MIGS-13

Source Material Identifier

CALU1027

Project relevance

comparative genomics

Growth conditions and genomic DNA preparation

P. hollandica CALU1027 was grown in the BG-11 medium [2]. The strain is a moderate mesophile, well growing at 20-22 °C under continuous flux of light. For DNA isolation cells were harvested by centrifugation and treated with 2 μg/mL Proteinase K in 0.1 M Tris-HCl (pH 8.5), 1.5 M NaCl, 20 mM Na2EDTA, and 2 % cetyltrimethylammonium bromide at 55 °C for 3-4 h. DNA was purified by standard protocol of organic extraction and ethanol precipitation.

Genome sequencing and assembly

For genome sequencing, DNA was randomly fragmented using Q800R sonicator system. After size selection, 500 bp DNA fragments were used for constructing sequence libraries and thereafter sequenced with a 250 bp paired-end reads method using the Illumina MiSeq platform according to the manufacturer’s protocol, resulting in 3,679,738 read pairs. Reads were processed via the Trimmomatic 0.32 tool [21] and after filtration there were 3,665,348 read pairs. The obtained reads were used for further genome assembly with SPAdes 3.5 [22]. From the resulting assembly, the P. hollandica CALU1027 contigs was selected and scaffolded with Contiguator 2.7.4 [23], using assembly GCF_000332315.1 as a reference. The draft genome of P. hollandica CALU1027 contained about 5.5 Mbp in 286 contigs organized in 10 scaffolds; the N50 length of the contigs was 33,173 and N50 length of the scaffolds - 1,244,169 bp (Table 3).
Table 3

Genome statistics

Attribute

Genome (total)

Value

% of totala

Genome size (bp)

5,525,469

100.00

DNA coding (bp)

3,931,877

71.16

DNA G + C (bp)

2,999,78

54.56

DNA scaffolds

10

Total genes

4,294

100.00

Protein coding genes

3,737

87.00

RNA genes

57

1.32

rRNA genes

12

0.28

tRNA genes

44

1.02

ncRNA genes

1

0.02

Pseudo genes

515

11.99

Genes in internal clusters

235

5.4

Genes with function prediction

2,770

64,5

Genes assigned to COGs

2,855

66.00

Genes with Pfam domains

2,386

55.56

Genes with signal peptides

86

2

Genes with transmembrane helices

869

20.24

CRISPR repeats

9

0.2

a The total is based on either the size of the genome in base pairs or the total number of protein coding genes in the annotated genome

Genome annotation

Protein-coding genes of draft genome assembly were predicted using the NCBI Prokaryotic Genome Annotation Pipeline (v.2.10) and an annotation method of best-placed reference protein set with GeneMarkS+ [24]. The annotated features were genes, CDS, rRNA, tRNA, ncRNA, and repeat regions. Functional assignments of the predicted ORFs were based on a BLASTP homology search against WGS of phylogenetically closest cyanobacteria and the NCBI non-redundant database. Functional assignment was also performed with a BLASTP homology search against the Clusters of Orthologous Groups (COG) database [25, 26]. As much as 2855 genes (66 %) were assigned as a putative function, and the remaining genes were annotated as either hypothetical proteins or proteins with unknown function.

Genome properties

The GC content of the P. hollandica CALU1027 genome was 54.56 %. Gene annotation revealed 3737 protein coding genes, 12 rRNA genes, and 44 tRNA genes. COG annotations of protein coding genes are presented in Table 4.
Table 4

Number of genes associated with general COG functional categories

Code

Value

% agea

Description

J

160

4.28

Translation, ribosomal structure and biogenesis

A

0

0

RNA processing and modification

K

141

3.77

Transcription

L

213

5.69

Replication, recombination and repair

B

3

0.08

Chromatin structure and dynamics

D

39

1.04

Cell cycle control, cell division, chromosome partitioning

V

64

1.71

Defense mechanisms

T

316

8.46

Signal transduction mechanisms

M

210

5.62

Cell wall/membrane biogenesis

N

56

1.50

Cell motility

U

76

2.03

Intracellular trafficking and secretion

O

144

3.85

Posttranslational modification, protein turnover, chaperones

C

148

3.96

Energy production and conversion

G

126

3.37

Carbohydrate transport and metabolism

E

201

5.37

Amino acid transport and metabolism

F

67

1.79

Nucleotide transport and metabolism

H

156

4.17

Coenzyme transport and metabolism

I

55

1.47

Lipid transport and metabolism

P

136

3.64

Inorganic ion transport and metabolism

Q

52

1.39

Secondary metabolites biosynthesis, transport and catabolism

R

407

10.89

General function prediction only

S

409

10.94

Function unknown

8

0.21

Not in COGs

aThe total is based on the total number of protein coding genes in annotated genome

Insights from the genome sequence

The assembly and analysis of P. hollandica CALU1027 genome annotation revealed a repertoire of genes necessary for the autonomous energy and substrate metabolism: 743 detected genes with relevance to 129 metabolic pathways have orthologs in P. hollandica CALU1027 and other cyanobacteria (Table 5). Comparative genomes analysis of P. hollandica CALU1027 with filamentious heterocystous cyanobacteria Anabaena variabilis ATCC29413 and unicellular prochlorophytes Prochlorococcus marinus CCMP1375 and Acaryochloris marina MBIC11017 revealed that the main differences were in the amino acids compounds, carbohydrates metabolism, membrane transport and stress response systems (data not shown).
Table 5

Selected functional capacities

Cell function

Metabolic system/element

Putative gene/gene product

Light energy metabolism

Oxygenic phototrophy; photorespiration

psaA-F, psaJ-L, psaX, psbA-D, psbH-P, psbU, psbV, psbW, psbZ, pcbA-C; ycf39, petA, petB, pet D, petE, hoxH/hoxY, PsbF, cyt f, cyt b 6; PC, CAT, SGAT, Fd-GOGAT, IpdA

Dark energy metabolism

Glycolysis and gluconeogenesis; methylglyoxal metabolism, pentose phosphate pathway; Entner-Doudoroff pathway; pyruvate cleavage; TCA with glyoxylate bypass

GlcK, HxK, PPgK, PfK1, PfK2, PPiFKa, PPiFKb, Fbp_I, B, X; Fba1- 2, TpI, GADH, G3PNP, PgK, PgM, EnO, PyK, PpS, PpD, Hyp1, GPDH; MgsA, GloA-B, AldA-B, GRE2; GPDH, PLG, RisA-B, TK, TA, FPK, XPK, PglD, OpcA; AlaDH, AlaR, AlaGAT, SerD, SerT; glcB-F, HxK, GoxR, HpyrR, GalDH, AldDH, 2PGP; PyK, PpS, PpD, Pc, PEPC, ME; PDE, POX, PDC, PFORa-d, PDHA-B, DDH, OPOT, ADHA; GOX, lysR

Lipid/pigments metabolism

Chl, iron tetrapyrrols, fatty acids, isoprenoids, phospholipids

PMgCD, PMgCH, PmgMT, ChlEAe, DVR, ChlB, ChlG, ChlL-M, POR; GltR, UroM, UroD, HemQ, HemX-Y; FabA-T, HpnE-H; CruA-G, CrtL, GlyP, GarL

Carbon substrate intermediary metabolism

Calvin cycle; fructose, galactose, mannose, sucrose, polyglucoside, aminosugar, nucleotide sugar, C1-substrate and glycogen metabolism

PRK, Rbc, PGK, GAPDH, TPI, FBA1-2, FBP_I-X, TK, RPE; cbbL; cbbS, Ss, RBCS, RBCI, ClCP, CA; ManA-P, MalE-G, K; MsmK, LamB, MalL-K, MalA-B; NAGK1-3, NagA-E, CbSA, ChbA-C; mtdA, FTCLI; GAT_C, GAT_D, GS, GBr, GP, MP, MOTs, aAMP

Nitrogen substrate intermediary metabolism

Nitrogen and ammonia assimilation; urea cycle

cynT, cynR, cynS, cynX; nrfB-H, niR1-3, niTa-Tc, narC, narG, narH, narI, napA-L, napR-T, nrfE-G, nrfX, GsI, GSIII, GlnE, GlnD, GOGDP1, GOGDP2, GlxC-D, GOGD, GAT, NRI, NRII, PII, PIIK, NtcA; UreD-G

Protein metabolism

Amino acids, polyamines and glutathione biosyntheses; protein processing, degradation, modification and folding; selenoproteins

GltB, GlxC-B, GldH, AspA-C, AsnA-B, GltS, GlsA, HisA-I, AstA-E, ArgR, SpeA-C, ArcA-D, MetN-T, ThrA-C, AspC, CysB-E, Lys1, LLP, CadA-C, DavA-D, CodA, LeuA-D, TrpA-E, TyrA, PheA, ProA-C, SelD, GlyA-B, AlaB, AlaR, CsdA, SufS, SerA-C; SelA-B

Mineral substrate metabolism

Phosphate, sulfur, iron and potassium metabolism

pho regulon; high-affinity phosphate transporter genes; siderophores; bacterioferritins; CysA, CysQ, SAT1-2, APSR, ASK, SIRFP, FPR_A; FhuB; kdpA-E, KefA-B, KefF

Enzyme cofactor metabolism

Coenzyme B12, FAD, FMN, lipoic acid, Mo-cofactor, NAD, pterines, pyridoxin, quinone, riboflavin, thiamine biosynthesis

BioC, BioH, HoxE, HoxF, HoxH, HoxU, HoxY, CobA-C, CbiA-K, ThiB-G; UbiA-H; menA-D; PyrD, PyrR, PyrP, RSAe, FMNAT, LUMP, RK, RSA, gapA, pdxA-K, FolA-B; LipA-C, LipL-M, BirA, GlyP, PdhB, SucB, AceB, BkdB

Secondary metabolism

Auxin, flavonoids, terpenes and derivatives biosynthesis

plant hormones (AUX1, APRT, PRAI, IGS,TSa, TM, IAH, IAD, AAD, AFTS), toxin-antitoxin replicon stabilization systems (RelB, E, F; CcdA-B, ParE-D, HigA-B, VapC-B, YoeB, YefM, YafQ, DinJ, YeeU, YkfI, YafW, YpjF, YgiZ)

Membrane transport

 

ABC transporters (phnC-E, oppA-F, dppA-F), FtsY, TatA-E, MgtA-E, YcnL-K, CopC-D, CsoR, CopA, ModB; TolA, TonB, NikQ, NikM, CbiQ, CbiO, CbiM, BioM, BioN, MtsA-C, YkoC-E lipT, Sec-translocase; secretion protein type E, type IV pilus (pilA, pilT)

Cell division, cytoskeleton

 

ftsZ, ftsW, ftsB, ftsL, ftsA, ZipA, ZapA, MinC-E, ParA-B, Maf, YgiD, YeaZ(TsaB); MreB-D, RodA, MraZ

Regulation

 

kaiA-C, sasA, CikA, Pex, CPM; nrrA, groEL, grpE, dnaJ, LdpA, PSF, SigB, RsbR-W, PemK, SigF, SigG, SigFV, sig70, hetR, TyrR, IcsR, YbeD, cAMPB, FNR, CGA, dnaG, rpoD, exoY, pagA, AtxA, AtxR, hcnA-C, Clp2, ArsR, HisI, PyrC, FolE, HemB, CynT, CysS, YGR262c; SpoT, RelA, Rex, Fur_Zur, Fnr, gpp

Stress response

Protection from reactive oxygen species; oxidative and periplasmic stress

sodA-C, cyt c551 peroxidase, HP1; SoxS-R, OxyR, PerR, NnrS, AhpC, HemO, gshA-B, GltC, GltT, Rth, SOR, Rdx, ROO, NRO, AHR, grlA, EnvC, HbO, CHb, FHP, HmpX, Hfq, HflX-C; DegP-S, RseP, RseA-B, SurA, DegQ, HtrA

Phages, integrons and CRISPRs

SA bacteriophages 11, TFP1-2, TFAP, TFC, Lys1-8, LysA-B, Hol1-2, TransI, endolysin; integrons (Int1-2, Int4, InyIPac); CRISPR cmr-cluster (Cmr1-6, Csx11, NEO113, TM1812, Cas02710); CasReg, Cas1-7, Csh1-2, Csd1-2, Cse1-4, Csn1-2, Csy1-4, Csa1-5, Csm1-5, Cst1-2

Chl a/b-containing Prochlorothrix and Prochloron were long considered to have a common ancestry with chloroplasts of green algae and higher plants [27, 28]. However, P. hollandica and another prochlorophytes were shown to possess unique genes pcbA − pcbC coding chl a/b-LHC apoproteins and they are dissimilar from CAB apoprotein superfamily of chloroplast antenna [1930]. It is notable that we found some PS II proteins commonly absent in cyanobacteria but usually belonging to chloroplast in green algae and higher plants: PsbW (6.1 kDa, nuclear encoded), PsbT (5 kDa, nuclear encoded), PsbR (10 kDa) and PsbQ (16 kDa, oxygen evolving complex protein). We also found that P. hollandica contains an ortholog of hetR gene (key regulator of heterocyst differentiation) although all these filamentous non-heterocystous cyanobacteria are devoid of nitrogenase and other prerequisites for diazotrophy [31, 32].

Conclusions

The studying of P. hollandica CCAP1490/1T (CALU1207) genome is valuable for analyses of photosynthesis genes evolution and for comparative genomics of cyanobacterial adaptation.

Abbreviations

chl: 

Chlorophyll

HL: 

High light

LHC: 

Light-harvesting complex

LL: 

Low light

PBP: 

Phycobiliprotein

PS: 

Photosystem

Declarations

Acknowledgements

This work was financially supported by Russian Foundation for Fundamental Research (grant № 16-04-00174) and by St. Petersburg State University (grant № 1.38.253.2015). We gratefully acknowledge the technical help of St. Petersburg University «Resource Center for Microscopy and Microanalysis» and «Resource Center for Development of Molecular and Cell Technologies».

Authors’ contributions

NV, EC and AL designed and carried out the experiments. NV, MR and AP performed the data analysis and drafted the 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)
Department of Microbiology, Faculty of Biology, St. Petersburg State University
(2)
Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University
(3)
Center for Algorithmic Biotechnology, St. Petersburg State University

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