Genome features of moderately halophilic polyhydroxyalkanoate-producing Yangia sp. CCB-MM3
© The Author(s). 2017
Received: 19 September 2016
Accepted: 8 January 2017
Published: 23 January 2017
Yangia sp. CCB-MM3 was one of several halophilic bacteria isolated from soil sediment in the estuarine Matang Mangrove, Malaysia. So far, no member from the genus Yangia, a member of the Rhodobacteraceae family, has been reported sequenced. In the current study, we present the first complete genome sequence of Yangia sp. strain CCB-MM3. The genome includes two chromosomes and five plasmids with a total length of 5,522,061 bp and an average GC content of 65%. Since a different strain of Yangia sp. (ND199) was reported to produce a polyhydroxyalkanoate copolymer, the ability for this production was tested in vitro and confirmed for strain CCB-MM3. Analysis of its genome sequence confirmed presence of a pathway for production of propionyl-CoA and gene cluster for PHA production in the sequenced strain. The genome sequence described will be a useful resource for understanding the physiology and metabolic potential of Yangia as well as for comparative genomic analysis with other Rhodobacteraceae.
KeywordsYangia Rhodobacteraceae Matang mangrove Halophile Polyhydroxyalkanoate
Yangia is a genus of the Roseobacter group, within the family Rhodobacteraceae , order Rhodobacterales , class Alphaproteobacteria , thus far containing only one species Yangia pacifica [1, 2]. Members of the Roseobacter clade have been widely detected in marine environments, from coastal to open ocean and from surface of the water to abyssal depths . The type strain of Y. pacifica , DX5-10T was isolated from coastal sediment of the East China Sea of the Pacific Ocean . The accumulation of poly(3-hydroxybutyrate), P(3HB) in Y. pacifica DX5-10 was observed. Yangia sp. strain ND199 was recently reported to produce poly(3-hydroxybutyrate-co-3-hydroxyvalerate), P(3HB-co-3HV) from structurally unrelated carbon sources . So far, only few bacteria including Haloferax mediterranei , ‘ Nocardia corallinia’, Pseudomonas sp. EL-2, Rhodococcus sp. NCIMB 40126 and recombinant Escherichia coli can synthesize P(3HB-co-3HV) from single unrelated carbon sources [5–9]. The incorporation of 3HV into 3HB-based polymer increases the flexibility, impact resistance as well as ductility of the polymer  and makes the polymer suitable for many industrial applications.
Mangroves are highly productive ecosystems covering approximately 75% of the total tropical and subtropical coastlines. Apart from wood production, mangrove forests support a wide range of functions including coastline protection, nutrient cycling, habitat for endangered species, breeding ground for marine life and have been proven as natural barrier againt tsunami . Matang mangrove, Malaysia is widely regarded as the best-managed sustainable mangrove ecosystem in the world. Yangia sp. CCB-MM3, analyzed in the present study, was isolated from soil samples obtained from the Matang mangrove. The sampling location was situated in estuarine mangrove ecosystem that is under both the influence of marine condition and the flow of freshwater. Saline environments including estuaries and coastal marine sites have been focus of study for halophilic organisms that flourish in these habitats. Halophiles have attracted interest as candidates for bioprocessing because of their unique property including the ability to grow in high salt containing media, allowing fermentation processes to run contamination free under non-sterile condition .
At the time of writing, there are more than 300 genome assemblies from members of the family Rhodobacteraceae but the complete genome from the genus Yangia has not been reported. Here, we present the first complete genome of a Yangia representative and insight into the genes or pathways for polyhydroxyalkanoate (PHA) biosynthesis in this halophilic bacterium.
Classification and features
Classification and general features of Yangia sp. strain CCB-MM3
Species Yangia sp.
pH range; Optimum
Maltose, lactate, malate, arginine, glutamate
Genome sequencing information
Genome project history
Genome sequencing project information
PacBio SMRTbell 10 Kb library
PacBio RS II
Gene calling method
GenBank date of release
July 18, 2016
Source material identifier
Growth conditions and genomic DNA preparation
Yangia sp. CCB-MM3 cells for genome sequencing was grown in L-ASWM [0.05% tryptone, 2.4% (w/v) artificial sea water mix (Marine Enterprises International, USA), pH 7.6] under rotation at 30 °C . Genomic DNA extraction was performed using the DNeasy Blood and Tissue Kit (Qiagen, USA). The genomic DNA was quantified using Qubit 3.0 Fluorimeter (Life Technologies, USA) and visualized by agarose gel electrophoresis (0.7%).
To promote PHA biosynthesis in Yangia sp. CCB-MM3, one-stage cultivation was carried out. Pre-culture of strain CCB-MM3 was prepared by growing cells on moderate halophiles (HM) medium containing per litre: 45 g NaCl, 0.25 g MgSO4 .7H2O, 0.09 g CaCl2.2H2O, 0.5 g KCl, 0.06 g NaBr, 5 g peptone, 10 g yeast extract and 1 g glucose at 30 °C with rotary shaking at 200 rpm for 6 h. Subsequently, 3% (v/v) inoculum (OD600nm = 4) was transferred into HM-1 medium containing per litre: 45 g NaCl, 0.25 g MgSO4.7H2O, 0.09 g CaCl2.2H2O, 0.5 g KCl, 0.06 g NaBr, 0.25 g KH2PO4, 2 g yeast extract and 20 g glycerol . The culture was incubated at 30 °C, 200 rpm for 48 h before being harvested. PHA was extracted from lyophilized cells according to the method described previously . 1H nuclear magnetic resonance spectrum was obtained in deuterated chloroform solution of the PHA polymer (25 mg/mL) recorded on a Bruker spectrometer (Bruker, Switzerland) at frequency of 400 MHz.
Genome sequencing and assembly
Whole genome sequencing of Yangia sp. CCB-MM3 was performed using the PacBio technology. In short, a library was prepared following the PacBio 10 Kb SMRTbell library preparation protocol. The final library was size selected using Blue Pippin electrophoresis (Saga Science, USA). The library was sequenced using two SMRT cells on PacBio RS II platform using P6-C4 chemistry. The run generated 153,311 reads with an average length of 14.46 Kb and a total of 2.22 Gb data. Raw reads were filtered and de novo assembled using hierarchical genome-assembly process v2 protocol in SMRT Analysis v2.3.0 . Two rounds of genome polishing were performed using Quiver to improve the accuracy of the assembly.
The genome annotation was performed using the rapid annotation using subsystem technology . The predicted Yangia sp. protein sequences were compared against the clusters of orthologous groups database using BLASTP. Non-coding genes and miscellaneous features were predicted using tRNAscan-SE , SignalP , TMHMM  and CRISPRFinder .
Genome composition for Yangia sp. CCB-MM3
% of total
Genome size (bp)
DNA coding (bp)
DNA G + C (bp)
Protein coding genes
Genes in internal clusters
Genes with function prediction
Genes assigned to COGs
Genes with Pfam domains
Genes with signal peptides
Genes with transmembrane helices
Number of genes associated with general COG functional categories
Translation, ribosomal structure and biogenesis
RNA processing and modification
Replication, recombination and repair
Chromatin structure and dynamics
Cell cycle control, cell division, chromosome partitioning
Signal transduction mechanisms
Cell wall/membrane biogenesis
Intracellular trafficking and secretion
Posttranslational modification, protein turnover, chaperones
Energy production and conversion
Carbohydrate transport and metabolism
Amino acid transport and metabolism
Nucleotide transport and metabolism
Coenzyme transport and metabolism
Lipid transport and metabolism
Inorganic ion transport and metabolism
Secondary metabolites biosynthesis, transport and catabolism
General function prediction only
Not in COGs
Insights from the genome sequence
Carbohydrate active enzymes (CAZy) in the genome of Yangia sp. CCB-MM3
No. of genes
No. of genes
Carbohydrate binding module
No. of genes
No. of genes
Glycoside hydrolase genes in the genome of Yangia sp. CCB-MM3
Glycogen debranching enzyme
Glycogen debranching enzyme
Lytic murein transglycosylase
Tail length tape measure protein
Type I secretion protein
Type I secretion protein
Glycosyl hydrolase family 88
Some species from the Roseobacter clade have been characterized as essential players in biogeocycling of organic or inorganic sulfur-containing compounds [23–25]. The genome of Yangia sp. CCB-MM3 encodes the enzymes necessary for assimilatory sulfate reduction including sulfate adenyltransferase (AYJ57_25280), adenylnylsulfate kinase (AYJ57_25275), phosphoadenylylsulfate reductase (AYJ57_02835) and sulfite reductase (AYJ57_02830). Interestingly, CCB-MM3 genome also harbours the complete set of sulfur-oxidizing genes including soxX (AYJ57_01935), soxY (AYJ57_01940), soxZ (AYJ57_01945), soxA (AYJ57_01950), soxB (AYJ57_01955), soxC (AYJ57_01960) and soxD (AYJ57_01965) for thiosulfate oxidation in vitro. SoxYZ is the carrier protein that interacts with SoxAX, SoxB and SoxCD; SoxAX cytochrome complex is proposed to link sulfur substrate to SoxYZ; dimanganese SoxB removes oxidized sulfur residue from SoxYZ through hydrolysis; and SoxCD catalyzes the oxidation of reduced sulfur residue bound to SoxYZ [26–29]. These genes encoding essential components of the Sox multienzyme complex are organized in a single locus in CCB-MM3. Analysis of Yangia sp. CCB-MM3 genome also revealed that rodanese-like sulfurtransferases (AYJ57_05465, AYJ57_08495, AYJ57_10220, AYJ57_16970 and AYJ57_24415) that can participate in the metabolism of thiosulfate and elemental sulfur during disproportionation are present in the genome.
Although the ability of Yangia to grow with free nitrogen gas as sole nitrogen source has not been analyzed yet, all genes necessary for nitrogen fixation were identified in the genome of Yangia sp. CCB-MM3. The genome encodes the subunits α and β of molybdenum-iron nitrogenase (AYJ57_00195, AYJ57_00200), its regulatory and accessory proteins (AYJ57_00310, AYJ57_00210, AYJ57_00215 and AYJ57_00315).
Genes involved in PHA metabolism in Yangia sp. CCB-MM3
No. of genes
Propionyl-CoA supplying pathway
PHA biosynthetic pathway
NADPH-dependent acetoacetyl-CoA reductase
Other aspect of PHA metabolism
PHA synthesis regulator
The formation of P(3HB-co-3HV) from its precursors, acetyl-CoA and propionyl-CoA is catalyzed by three enzymes  and the genes encoding these enzymes were identified in the genome of CCB-MM3. The first reaction consists of either the condensation of two acetyl-CoA or condensation of acetyl-CoA and propionyl-CoA by β-ketothiolase encoded by multiple phaA in CCB-MM3 (AYJ57_07995, AYJ57_09725, AYJ57_11220, AYJ57_15015 and AYJ57_20090). The resulting intermediate is reduced to 3-hydroxybutyryl-CoA or 3-ketovaleryl-CoA by NADPH-dependent acetoacetyl-CoA reductase encoded by phaB (AYJ57_01725, AYJ57_11215 and AYJ57_24165). The hydroxyacyl-CoA monomers are then incorporated into the growing polymer chain by PHA synthase, encoded by phaC . The genome of Yangia sp. CCB-MM3 possesses two PHA synthases genes, phaC1 Ys and phaC2 Ys (AYJ57_06535 and AYJ57_14600) that are located on chromosome 1 and 2, respectively. Both phaC1 Ys and phaC2 Ys encode 598 amino acid proteins which show 67 and 81% identity with phaC from Citreicella sp. SE45. These PHA synthases belong to Class I that have only one subunit and show preference to short chain length hydroxyacyl-CoA monomers .
Besides genes that are directly involved in PHA biosynthesis, gene involved in other aspect of PHA metabolism e.g. PHA depolymerase (phaZ) was annotated in the genome of Yangia sp. CCB-MM3. Since PHA is accumulated as storage compound for its producer, some PHA-producers harbour native machinery for the degradation of PHA. The synthesized PHA is catabolized by intracellular PhaZ and subsequently reutilized by cell . However, mechanism of control for PHA biosynthesis or degradation in its native producer is not yet fully understood. Two PHA depolymerases, phaZ1 Ys and phaZ2 Ys (AYJ57_12275 and AYJ57_14595) were found in CCB-MM3. Another noncatalytic PHA granule-associated protein, phasin, was found to be encoded by single copy of phaP gene (AYJ57_14605) in CCB-MM3. Phasin has putative role in maintaining the stability of PHA granules formed by preventing the coalescence of separated granules . The transcriptional repressor gene phaR (AYJ57_10595) that encodes for protein that regulates the transcription of phaP was also annotated in CCB-MM3 genome. It was proposed that PhaR functions as a repressor protein of transcription by binding to the upstream region of PhaP .
At least 300 members of the family Rhodobacteraceae have publically accessible genomes. Yangia sp. CCB-MM3, however, represents the first sequenced genome from the genus. The strain was selected for genome sequencing by our research group as part of a study focusing on characterizing the microbiome of Malaysia mangrove sediments. The strain CCB-MM3 genome includes genes encoding monomer supplying and biosynthetic pathway for PHA production. Availability of the genome sequence will facilitate further study on the strain’s biological potential and provide reference material for comparative genomic analysis with other Rhodobacteraceae .
Carbohydrate binding module
Clusters of orthologous groups
Hierarchical genome-assembly process
Moderate halophiles medium
Low nutrient artificial seawater medium
Rapid annotation using subsystem technology
Single molecule real-time
This project was funded by the Research University (RU) mangrove project grant (1001/PCCB/870009). N.-S. Lau thanks Universiti Sains Malaysia for the post-doctoral fellowship support.
NL wrote the manuscript, assembled and annotated the genome. KS performed the laboratory experiments. AAA coordinated the study and the manuscript drafting. All authors read and approved the final manuscript.
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.
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