Complete Genome Sequence of Pseudomonas chloritidismutans 6L11 with Plant Growth-Promoting and Salt-Tolerant Properties.

HomeMolecular Plant-Microbe Interactions®Vol. 35, No. 9Complete Genome Sequence of Pseudomonas chloritidismutans 6L11 with Plant Growth–Promoting and Salt-Tolerant Properties PreviousNext RESOURCE ANNOUNCEMENT OPENOpen Access licenseComplete Genome Sequence of Pseudomonas chloritidismutans 6L11 with Plant Growth–Promoting and Salt-Tolerant PropertiesDandan Zhou, Zhiqiu Yin, Xujian Li, Yanru Cui, Qi Cheng, Binghai Du, Kai Liu, Chengqiang Wang, and Yanqin DingDandan Zhouhttp://orcid.org/0000-0003-1423-5436College of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Zhiqiu YinNational Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Shandong Agricultural University, Tai'an 271018, ChinaCollege of Resources and Environment, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Xujian LiCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Yanru CuiCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Qi ChengCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Binghai DuCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaNational Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Kai LiuCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, Chengqiang Wang†Corresponding authors: C. Wang; E-mail Address: wangcq@sdau.edu.cn, and Y. Ding; E-mail Address: dyq@sdau.edu.cnCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaNational Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this author, and Yanqin Ding†Corresponding authors: C. Wang; E-mail Address: wangcq@sdau.edu.cn, and Y. Ding; E-mail Address: dyq@sdau.edu.cnCollege of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, ChinaNational Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Shandong Agricultural University, Tai'an 271018, ChinaSearch for more papers by this authorAffiliationsAuthors and Affiliations Dandan Zhou1 Zhiqiu Yin2 3 Xujian Li1 Yanru Cui1 Qi Cheng1 Binghai Du1 2 Kai Liu1 Chengqiang Wang1 2 † Yanqin Ding1 2 † 1College of Life Sciences and Shandong Engineering Research Center of Plant-Microbial Restoration for Saline-alkali Land, Shandong Agricultural University, Tai'an 271018, China 2National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources, Shandong Agricultural University, Tai'an 271018, China 3College of Resources and Environment, Shandong Agricultural University, Tai'an 271018, China Published Online:14 Sep 2022https://doi.org/10.1094/MPMI-01-22-0029-AAboutSectionsView articlePDFSupplemental ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmailWechat View articlePseudomonas chloritidismutans is a facultative anaerobic and chlorate-reducing bacterium. Many strains of chlorate-reducing P. chloritidismutans are suitable for biotechnological applications because they can undergo ammonia assimilation, aerobic denitrification, phosphorus removal, and pollutant degradation (Hou et al. 2021; Wolterink et al. 2002). Chlorate-reducing bacteria were mostly isolated from domestic sewage and industrial wastewater (Bansal et al. 2009). The current research on chlorate-reducing P. chloritidismutans has focused mainly on the degradation of some water pollutants such as chlorate, bromate, and nitrate. The characteristics, activities, and mechanisms of relevant reductases involved in the degradation process of P. chloritidismutans have also been studied. A strain P. chloritidismutans AW-1 was first isolated from the biomass of an anaerobic chlorate-reducing bioreactor in 2002 (Wolterink et al. 2002); then, the strain P. chloritidismutans K14 was separated from aquaculture sediments (Hou et al. 2021). A chlorate reductase with the ability to reduce chlorate and bromate has been purified from P. chloritidismutans AW-1 (Wolterink et al. 2003). Genome and proteome analysis revealed the constitutive presence of chlorate reductase and chlorate dismutase in strain AW-1 (Mehboob et al. 2016). Strain AW-1 was found to degrade n-alkanes via oxygenase-dependent pathways and to simultaneously degrade halogenates and reduce chlorates (Mehboob et al. 2009; Peng et al. 2017). This indicates that P. chloritidismutans may have a certain significance for the natural halogen cycle of aquatic and terrestrial ecosystems. Thus far, only two draft genome sequences, those of P. chloritidismutans AW-1 and P. chloritidismutans GOM4, have been reported (Mehboob et al. 2016) and the complete genome sequence of this species is unclear, which limits the genetic understanding of P. chloritidismutans. In this study, P. chloritidismutans 6L11 was isolated and analyzed for plant growth–promoting and salt-tolerant properties, which may facilitate its use in agricultural production.P. chloritidismutans 6L11 was recently isolated from the saline-alkaline rhizosphere soil of Salicornia L. in Shandong, China. The study of strain 6L11 has revealed newly discovered functions of P. chloritidismutans as a plant growth–promoting rhizobacterium (Supplementary Fig. S1). P. chloritidismutans 6L11 is a Gram-negative, rod-shaped, facultative anaerobic strain, and it has been confirmed to be capable of producing auxin, protease, and iron carriers and dissolving organic phosphorus and potassium. Strain 6L11 has growth-promoting and salt-tolerant effects on wheat in saline-alkaline soil (Supplementary Fig. S1).To further study the functional genes and specific mechanisms of P. chloritidismutans for growth-promoting and salt-tolerant function, we performed whole-genome sequencing of strain 6L11. As of now, this is the first complete genome sequence of species P. chloritidismutans. Complete genome sequencing of strain 6L11 was performed using the platforms Illumina MiSeq and PacBio Sequel. Two libraries were constructed. A 2 × 150-bp paired-end library of platform Illumina MiSeq was prepared using the TruSeq Sample Prep Kit with an insert fragment 400 bp in length. A PacBio library was prepared using a Template Prep Kit 1.0 with an insert fragment of 20 kb. We obtained a total of 8,175,614 and 114,115 reads from platforms Illumina MiSeq and PacBio Sequel, respectively. The quality of the second-generation sequencing data was assessed with FastQC (Patel and Jain 2012), and the 3′ end adapters were removed using AdapterRemoval (Schubert et al. 2016). The coverage of the sequence reached 271× . All reads passed through the Illumina MiSeq platform were corrected by SOAPec based on the k-mer frequency (k-mer setting value is 17) (Luo et al. 2012). The filtered reads were assembled using SPAdes (Bankevich et al. 2012) to build scaffolds and contigs. Canu software (Koren et al. 2017) was used to assemble the data obtained by PacBio platform sequencing. All assembled results were integrated to generate a complete sequence. Finally, the complete genome sequence of P. chloritidismutans 6L11 was acquired after the rectification using Pilon software (Walker et al. 2014). The genome sequence, gene prediction, and noncoding RNA (ncRNA) prediction information were first integrated into a standard GBK (GenBank) format file; then, the circle map of this genome was drawn using CGView (Stothard et al. 2005). Finally, the map was edited using Photoshop CS. For example, the chr sequence was plotted as a genomic circle map (Fig. 1A).Fig. 1. A, Genomic circle map and B, Clusters of Orthologous Groups of proteins (COG) annotation of Pseudomonas chloritidismutans 6L11. From inside to outside, the first circle represents the scale, the second circle represents GC skew, the third circle represents GC content, the fourth and seventh circles represent the COG to which each coding sequence (CDS) belongs, and the fifth and sixth circles represent the location of CDS, transfer RNA, and ribosomal RNA on the genome.Download as PowerPointA 4,466,844-bp circular chromosome of P. chloritidismutans 6L11 was obtained (Fig. 1A) and the GC content was found to be 63.0%. In total, 4,096 open reading frames were annotated, with an average length of 959 bp. The RNA genes included 12 ribosomal RNAs, 60 transfer RNAs, and 4 other ncRNAs. No plasmids or CRISPRs were found. The Clusters of Orthologous Groups of proteins annotation (Fig. 1B) results showed the proportion of different function genes in strain 6L11. The analysis identified a total of 73 genes associated with the biosynthesis, transport, and catabolism of secondary metabolites and 50 involved in defense mechanisms. There were 980 genes of unknown function. P. chloritidismutans AW-1 and GOM4 are two strains of P. chloritidismutans with high genomic similarity to 6L11 but the genome assembly levels of these three strains are different: the genome assembly level of AW-1 is contig, the genome assembly level of GOM4 is a scaffold, and only the assembly level of 6L11 is a complete genome. Strains 6L11, AW-1, and GOM4 were found to have similar GC content and coding gene numbers (Table 1). The three strains were subjected to comparative genomic analysis. Orthologous groups of protein families were delimited using OrthoFinder software (Emms et al. 2015). The common and unique gene families were extracted from the OrthoFinder output files. The result was visualized using the online interface of EVenn (Chen et al. 2021) (Supplementary Fig. S2). The genome of strain 6L11 had 3,492 genes in common with strains AW-1 and GOM4, and there were 192 unique genes (Supplementary Fig. S2). Most of the unique genes of strain 6L11 are flagella-related proteins, sulfate ABC transporters, and transcriptional regulators.Table 1. Statistical comparison of the genomes of Pseudomonas chloritidismutans strains 6L11, AW-1, and GOM4aNumber ofbStrainGenBank ID; assembly accession (NCBI)Size (bp)G + C (%)ContigsCDSrRNAtRNA6L11NZ_CP086067.1; GCA_020783375.14,466,84463.014,0961260AW-1NZ_AOFQ01000032.1; GCF_019702405.15,056,34962.5774,5721381GOM4NZ_JAHHFP010000011.1; GCF_019702405.14,615,17162.9294,186347aGenome information for each strain is according to the data obtained from NCBI.bCDS = coding sequences, rRNA = ribosomal RNA, and tRNA = transfer RNA.Table 1. Statistical comparison of the genomes of Pseudomonas chloritidismutans strains 6L11, AW-1, and GOM4aView as image HTML Using antiSMASH (6.0.1) (Blin et al. 2021), 10 biosynthetic gene clusters of secondary metabolites (e.g., carotenoid, desferrioxamine E, and ectoine) in strain 6L11 were predicted (Supplementary Fig. S3). These metabolites are suitable candidates for further biocontrol and biomedical application. However, no biosynthetic gene clusters of secondary metabolites were predicted in strains AW-1 and GOM4. This may indicate that 6L11 has considerable potential value in agricultural and biomedical applications. Through genomic comparison and analysis, it is predicted that there are many growth-promoting genes in strain 6L11. The growth-promoting genes contain the encoding gene gcd for quinone glucose dehydrogenase (LLJ08_RS14220 and LLJ08_RS16220) (Li et al. 2018) and the coenzyme PQQ synthesis genes pqqB (LLJ08_RS10820), pqqC (LLJ08_RS10815), and pqqE (LLJ08_RS10805 and cLLJ08_RS10850) that dissolve inorganic phosphorus (Yang et al. 2010); the alkaline phosphodiesterase synthesis gene phoD (LLJ08_RS02890) that dissolves organophosphate (Kageyama et al. 2011); the synthesis gene glpQ (LLJ08_RS02835 and LLJ08_RS07355) that produces glycerophosphodiesterase; the siderophore biosynthesis gene (LLJ08_RS02835) in the IucA/IucC family siderophore synthesis gene cluster (Carroll and Moore 2018); and the nitrogen fixation related genes iscU (LLJ08_RS05375), fixG (LLJ08_RS07015 and LLJ08_RS12130), and fixS (LLJ08_RS12145-LLJ08_RS12150) (Addo and Dos Santos 2020). There are also many genes involved in the synthesis of plant hormones in P. chloritidismutans 6L11, such as the amidase encoding gene amiE (LLJ08_RS14075) and the indole-3-pyruvate monooxygenase encoding gene YUC9 (LLJ08_RS14160) (a redundant gene of YUCCA) for indole-3-acetic acid synthesis (Oleńska et al. 2020), the pyrophosphate-encoding gene GGPS (LLJ08_RS02820) for gibberellin synthesis (Hedden and Thomas 2012), the key gene miaA (LLJ08_RS02965) for cytokinin synthesis, the gene GGPS (LLJ08_RS02820) for the synthesis of abscisic acid precursor substances geranylgeranyl pyrophosphate and farnesyl pyrophosphate, and the key gene ispH (LLJ08_RS163) for isopentenyl pyrophosphate synthesis. These genes are involved in the production of different plant hormones in P. chloritidismutans 6L11, and they could improve the growth of many agriculturally important plants (Bhattacharyya and Jha 2012; Kumar et al. 2018; Oleńska et al. 2020).A series of genes related to salt and alkali resistance and other stresses were predicted in P. chloritidismutans 6L11, including sodium-potassium pumps and genes for the synthesis of such compatible substances as betaine and trehalose, which regulate cellular osmotic pressure and mitigate damage to the bacterium from external saline stress (Gregory and Boyd 2021). These genes are conducive to the survival of P. chloritidismutans 6L11 under saline-alkaline conditions and could also enhance the growth of plants in a saline-alkaline environment. The five synthesis genes nhaA (LLJ08_RS07445), nhaD LLJ08_RS14740), NHA1 (LLJ08_RS00365), nhaP2 (LLJ08_RS02030 and LLJ08_RS09470), and czcD (LLJ08_RS13450 and LLJ08_RS15335) of Na+/H+ antiporter (Wu et al. 2019); an ACC deaminase synthesis gene PH0054 (LLJ08_RS12230) (Mayak et al. 2004); two synthesis genes betA (LLJ08_RS12615) and betB (LLJ08_RS12620) for betaine choline oxidation (Cánovas et al. 2000); and six genes otsA (LLJ08_RS04405), otsB (LLJ08_RS04400), treY (LLJ08_RS10485), treZ (LLJ08_RS10495), treS (LLJ08_RS10425 and LLJ08_RS18175), and treF (LLJ08_RS01825) in the trehalose synthesis pathway (MacIntyre et al. 2020) have been established. Furthermore, the three key genes ectA (LLJ08_RS19530), ectB (LLJ08_RS19535), and ectC (LLJ08_RS19540) involved in the synthesis of tetrahydropyrimidine (Kuhlmann and Bremer 2002) were also predicted and there is no related gene in the degradation pathway of tetrahydropyrimidine in strain 6L11 that can be used as a chassis cell in the industrial production of tetrahydropyrimidine for biomedical application (Frikha-Dammak et al. 2021). Carotene (violetin and neoxanthin) plays an important role in adversity stress (He et al. 2021). The gene ratio analysis showed that the same carotenoid synthesis gene cluster is present in both strain 6L11 and Enterobacteriaceae bacterium DC413 (Sedkova et al. 2005).Data AvailabilityThe chromosome sequence of P. chloritidismutans 6L11 has been deposited in GenBank under accession number CP086067. The BioSample and BioProject designations for this project are SAMN11866291 and PRJNA224116, respectively.AcknowledgmentsWe thank LetPub for its linguistic assistance during the preparation of this manuscript.Author-Recommended Internet ResourcesBioProject: https://www.ncbi.nlm.nih.gov/bioproject/PRJNA224116BioSample: https://www.ncbi.nlm.nih.gov/biosample/SAMN22746559DNA Data Bank of National Center for Biotechnology Information: https://www.ncbi.nlm.nih.gov/assembly/GCF_020783375.1The author(s) declare no conflict of interest.Literature CitedAddo, M. A., and Dos Santos, P. C. 2020. Distribution of nitrogen-fixation genes in prokaryotes containing alternative nitrogenases. ChemBioChem 21:1749-1759. https://doi.org/10.1002/cbic.202000022 Crossref, Medline, ISI, Google ScholarBankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. 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Copyright © 2022 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.DetailsFiguresLiterature CitedRelated Vol. 35, No. 9 September 2022ISSN:0894-0282e-ISSN:1943-7706 Download Metrics Article History Issue Date: 22 Sep 2022Published: 14 Sep 2022Accepted: 27 Apr 2022 Pages: 870-874 InformationCopyright © 2022 The Author(s).This is an open access article distributed under the CC BY-NC-ND 4.0 International license.Funding National Natural Science Foundation of ChinaGrant/Award Number: 31770115 Key R&D Program of Shandong ProvinceGrant/Award Number: 2021CXGC010804 Tai-Shan Scholar Program from the Shandong Provincial Government Keywordscomplete genome sequenceplant growth–promoting rhizobacteriumPseudomonas chloritidismutansrhizosphericsalt-tolerantThe author(s) declare no conflict of interest.PDF download