Abstract
A Gram-stain-negative, halotolerant bacterium designated as PTR5T was isolated from the roots of rice plants, collected in Ilsan, South Korea. Cells were, aerobic, asporogenous, motile, rod-shaped, white in color, and grew at 5–38 °C (optimum 30 °C), at pH 5.0-0-8.0 (optimum, 7.0) and tolerates up to 10% (w/v) NaCl (optimum, 0% NaCl). According to the EZbioCloud server the most closely related Devosia species to strain PTR5T based on 16 S rRNA gene sequence comparison are Devosia crocina (97.4%), followed by D. soli (97.2%), D. lucknowensis (96.9%) and D. marina (96.5%). The respiratory quinone was identified as Q-10. The major polar lipids were phosphatidylglycerol and diphosphatidylglycerol. C16:0, C18:1 ω7c 11-methyl and summed feature 8 (comprising C18:1 ω7c/C18:1 ω6c) constituted the main cellular fatty acids. The draft genome sequence of strain PTR5T was 3,689,283 bp in size. The average nucleotide identity (ANI), digital DNA–DNA hybridization (dDDH) and amino acid identity (AAI) values between strain PTR5T and its close relative were 72.8–76.8%, 19–20.7% and 70.3–75%, respectively. The G + C content was 63.7%. Strain PTR5T was able to produce siderophore and indole acetic acid (IAA) in the presence of l-tryptophan. Genes for siderophore production, auxin responsive and tryptophan biosynthesis were present in the genome of novel strain. Also, gene clusters involved in detoxification of various metal pollutants and antibiotics were also revealed in the genome of novel strain PTR5T, this suggest that novel strain can facilitate bioremediation of heavy metals and antibiotics in contaminated areas. This study aimed to determine the detailed taxonomic position of the strain PTR5T using the modern polyphasic approach. On the basis of evidence presented in this study, strain PTR5T is considered to represent a novel species of the genus Devosia, for which the name Devosia oryzisoli sp. nov. (type strain PTR5T (KCTC 82691T = TBRC 15163T) is proposed.
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Introduction
The genus Devosia has been created by the reclassification of Pseudomonas riboflavina as Devosia riboflavina (Nakagawa et al. 1996). Until April 2022, the genus Devosia comprises 32 species with validly published names″ (https://lpsn.dsmz.de/genus/devosia). Members of the genus are ubiquitous in diverse ecological niches including nitrifying inoculum (Vanparys et al. 2005), roots of rice plant (Chhetri et al. 2022), hexachlorocyclohexane dump sites (Dua et al. 2013), soil (Yoon et al. 2007), deep sediment (Jia et al. 2014), beach sediment (Lee et al. 2007), medical leech (Galatis et al. 2013) and alpine glacier (Zhang et al. 2012). Members of the genus Devosia are described as Gram-negative, flagellated, rod-shaped, obligately, contains Q-10 or Q-11 as the predominant respiratory quinone and have diverse colony colors like yellow, white, yellow-brown, orange and cream. Members of the genus Devosia are best studied for their potential to degrade several toxic compounds, establishing their promising candidature for bioremediation (Sato et al. 2012). Mycotoxins are fungal metabolites toxic to animals and can be accumulated in crop plants and creates a health risk for humans and livestock. Many toxins like fumonisins and trichothecenes are heat-stable and cannot be deactivated by cooking. Previous studies showed that many bacteria isolated for the degradation of deoxynivaleonol (DON) were identified as Devosia strains (Wang et al. 2019). In our recent study we isolated two members of genus Devosia found to produce siderophore and auxin (Chhetri et al. 2022). In the present study, we again isolated a novel species of genus Devosia, examined the amounts of IAA produced, detected the siderophore synthesis abilities and examined its taxonomic positions by a polyphasic approach including genome analysis. Genome sequencing allowed us to identify genes that might be involved in its plant growth-promoting (PGP) capacity. The annotated genome sequence of novel strain revealed vital gene clusters involved in exopolysaccharide synthesis, toxin-antitoxin system, and resistant against various antibiotics and metals, which are of considerable biotechnological value.
Isolation and cultivation
Strain PTR5T was isolated from the sterilized roots of fresh rice plants in Ilsan, South Korea, (GPS positioning of the sample collection site; 37°40′26.4″ N 126°48′20.88″ E). The samples were washed with tap water, and then immersed in 70 % alcohol for 3 min and washed 3 times with sterile water. The root samples were then ground in a sterile pottery mortar, which produced a suspension including bacteria from the rhizoplane and from the inner tissues of the roots. Subsequently, the suspension was diluted with double-distilled water using the standard dilution plating technique and then incubated at 28 °C on Reasoner’s 2 agar (R2A; Difco) for one week (Kim et al. 2019a). A single colony was chosen based on different morphology from the plates, purified by repeated streaking and transferred to new R2A plates. Selected colonies were sent to Bionics (Daejeon, Republic of Korea) for 16 S rRNA gene analysis. The isolate was preserved in 50% (v/v) glycerol at − 80 °C. Strain PTR5T has been deposited in the Korean Collection for Type Cultures (KCTC, Korea) and Thailand Bioresource Research Center (TBRC).
16 S rRNA gene phylogeny
TaKaRa MiniBEST Bacteria Genomic DNA extraction Kit version 3.0 (TaKaRa) was used for extraction of genomic DNA in accordance with the manufacturer’s instructions. The 16 S rRNA gene of the isolate was directly amplified by colony-PCR using four universal bacterial primers 27 F, 518 F, 805R and 1492R; PCR products were commercially sequenced (Solgent, Korea). The almost complete sequence (1354 nt) of the 16 S rRNA gene of strain PTR5T determined in this study was compared, using the CLUSTALX 2.1 programme (Thompson et al. 1997), with those of representatives of the genus Devosia and multiple sequences were aligned using MEGA 7.0 software (Kumar et al. 2016). Phylogenetic analyses were analysed with neighbor-joining (NJ) (Saitou and Nei 1987), maximum-likelihood (ML) (Felsenstein 1981) and maximum-parsimony (MP) (Fitch 1971). Evolutionary distances were calculated using Kimura’s two-parameter model (Kimura 1980) and the robustness of the topology in the phylogenetic trees was evaluated by bootstrap analyses based on 1000 resamplings (Felsenstein 1985).
Genomic features
The draft genome of strain PTR5T was sequenced using the Illumina HiSeq platform by Macrogen Co., Ltd. (Seoul, Republic of Korea) and assembled using the SOAPdenovo version 3.10.1 de novo assembler. For genome sequencing of strain PTR5T, a standard DNA library was prepared using the TruSeq DNA PCR-Free kit library (Illumina). Barrnap (0.9-dev) (https://github.com/tseemann/barrnap) was used for further validation of the 16 S rRNA gene (1454nt) in the genome, and both results yielded identical results. The genomic DNA G + C content was determined directly from the draft genome sequence. The ANI, dDDH and AAI values between the strain PTR5T and closely related members were analysed using the online webservers (www.ezbiocloud.net/tools/ani) (Yoon et al. 2017), (http://ggdc.dsmz.de) (Meier-Kolthoff et al. 2013) and (http://enve-omics.ce.gatech.edu/aai/), respectively. For the AAI values, protein sequences were predicted from genomic sequences using GeneMarksS. The CheckM bioinformatics tool was used to assess genome contamination and completeness (https://ecogenomics.github.io/CheckM) of strain PTR5T (Parks et al. 2015). The function of coding genes in the assembled genome were annotated by using server database called evolutionary genealogy of genes: Nonsupervised Orthologus Groups (eggnog) 4.5 (Huerta-Cepas et al. 2016). Whole genome sequences of close strains were downloaded from NCBI and a phylogenomic tree based on the concatenation of 92 core genes was constructed by using UBCG (Na et al. 2018). Genes involved in secondary metabolism were predicted by antibiotics and Secondary Metabolite analysis shell (antiSMASH) version 5.0 (Blin et al. 2019). Genome annotation was conducted by the NCBI prokaryotic genome annotation pipeline (PGAP) (Tatusova et al. 2016) and Rapid Annotation using Subsystem Technology (RAST) server (Aziz et al. 2008).
Physiology and chemotaxonomy
Based on 16 S rRNA gene sequence similarities and phylogenetic trees analysis results, D. crocina KACC 14,589T, D. soli KACC 11,509T, D. subaequoris KACC 14,985T, D. lucknowensis DSM 25,398 and D. riboflavina KACC 11,387T were selected as reference strains and were evaluated together with strain PTR5T under identical experimental conditions. The phylogenetically related type strains, D. soli KACC 11,509T, D. crocina KACC 14,589T, D. subaequoris KACC 14,985T, D. riboflavina KACC 11,387T and D. lucknowensis DSM 25,398 were purchased from Korean Agricultural Culture Collection (KACC) and Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSM) and used as reference strains for physiological tests and fatty acid detection. Cell morphology of strain PTR5T was observed on R2A agar after 48 h of incubation at 30 °C. Cells were observed under transmission electron microscope (TEM) (LIBRA 120, Carl Zeiss, Germany), using cells grown in R2A at 30 °C. For TEM preparation, the cells were suspended in distilled water and a grid was placed on the suspension for one minute, followed by negative staining of the cells with phosphotungustic acid (PTA). Gram staining was performed according to the procedure described previously (Kim et al. 2019b). Motility was evaluated in R2A medium containing 0.4% agar. Growth under anaerobic conditions was observed by incubating the cells in a GasPak jar (BBL, Cockeysville, MD, USA) at 30 °C for 10 days. Catalase activity was determined by bubble formation in 3% (v/v) H2O2, while oxidase activity was analysed by oxidation of 1% (w/v) tetramethyl-p-phenylenediamine (bioMérieux). Tolerance of the cells to various NaCl concentrations was tested in R2A broth containing 0–10% NaCl (w/v, at 0.5% intervals) as described previously (Chhetri et al. 2020). Growth at different temperatures (3, 5, 10, 18, 30, 35, 38, 42, and 45 °C) and various pH values (pH 4.5–11.0 at intervals of 0.5 pH units) was assessed after 7 days of incubation. Growth of strain PTR5T was monitored for 7 days on R2A agar under different temperatures (3, 5, 10, 18, 30, 35, 38, 42, and 45 °C). The pH range was assessed by cultivating cells in R2A broth adjusted to pH 4.0–10.0 (at 1.0 pH unit intervals) using citrate/NaH2PO4 buffer (pH 4.0–5.0), phosphate buffer (pH 6.0–8.0), Tris buffer (pH 9.0–10.0) and Sodium phosphate buffer (pH 11.0) at 30 °C for 7 days. Growth was evaluated at 30 °C on several standard bacteriological media: R2A agar, MA (marine agar), trypticase soy agar (TSA), nutrient agar (NA) and Luria Bertani agar (LB; all from Difco). The presence of flexirubin-type pigments was investigated using 20% (w/v) KOH solution (Kim et al. 2020). Extraction of cells for carotenoid analysis were achieved with a 10 ml methanol/acetone mixture (1:1, v/v) and the absorption spectrum of the pigments was assessed with a spectrophotometer (Multiskan GO; Thermo Fisher Scientific) (So et al. 2022).
Hydrolysis of chitin, CM cellulose, starch, and casein was determined as previously described (Kim et al. 2019a). Hydrolysis of Tween 80, Tween 60 and Tween 40 was examined as described by Smibert and Krieg (1994). Additional biochemical tests for strain PTR5T and its reference strains were performed using API ZYM and API 20 NE kits according to the methods described by the manufacturer (bioMérieux) under equivalent test conditions.
For cellular fatty acid analysis, cells of strain PTR5T and other reference strains were grown on R2A medium broth at 30 °C and were collected at late-exponential phase. Cells were extracted by saponification, methylation and extraction, as reported previously (Kuykendall et al. 1988). The Sherlock Microbial Identification System V6.01 (MIS, database TSBA6, MIDI Inc., Newark, DE, USA) was used to identify the extract.
Respiratory quinone was extracted with chloroform/methanol (2:1, v/v), evaporated under a vacuum, re-extracted with acetone and analyzed using high-performance lipid chromatography (HPLC) in accordance with the protocol described in previous reports (Collins and Jones 1981).
The polar lipids were extracted as described previously (Minnikin et al. 1984) and analyzed by two-dimensional thin-layer chromatography using chloroform/methanol/water (65:25:4; v/v/v) in the first dimension and chloroform/methanol/acetic acid/water (80:15:12:4; v/v/v/v) in the second dimension. Appropriate detection reagents were used to identify the spots (Komagata and Suzuki 1987; Kang et al. 2021).
Indole acetic acid (IAA), siderophore production and nitrogen fixation
Strains PTR5T was grown in R2A broth with or without 0.1% tryptophan for 5 days at 30 °C. After 5 days of incubation the cells were centrifuged at 6000 rpm for 30 min. 1ml of supernatant was transferred and mixed with 2ml of Salkowski’s reagent (2% 0.5 M, FeCl3 in 35% HClO4 solution), and incubated at room temperature for 30 min, and spectrophotometrically assessed at 530 nm. IAA production was quantified by using a standard curve with known concentrations of pure commercial IAA. Uninoculated R2A broth was treated as a negative control. Change in pink color indicated the production of IAA. The results were compared with and without l-tryptophan as described previously (Chhetri et al. 2022). Strain PTR5T was examined for siderophore production on Chrome Azurol S (CAS) plates. Strain PTR5T was spot inoculated and incubated at 30 °C for 5 days. Since the strain PTR5T was isolated from the roots of rice plants its nitrification ability was also assessed. Jensen’s nitrogen free medium was used for this purpose, and bromothymol blue (BTB) was used as an indicator. Growth of strain PTR5T in nitrogen free medium was observed for one week. All experimental analyses were performed in triplicate to ensure reproducibility.
Results and discussion
16 S rRNA gene sequence similarities and phylogenetic analysis
The 16 S rRNA gene sequence analysis in the EzBioCloud database showed that, strain PTR5T was closest to D. crocina KACC 14,589T (97.4%), followed by D. soli KACC 11,509T (97.2%), D. subaequoris KACC 14,985T (97.2%) and D. lucknowensis DSM 25,398 (96.2%), D. submarina KMM 9415T (96.5%) and D. riboflavina KACC 11,387T (96.4%). The 16 S rRNA sequence similarities among the strain PTR5T and other species of the genus were 94.0-97.4%. In neighbor-joining tree, strain PTR5T formed an independent lineage within the genus Devosia close to D. soli KACC 11,509T, D. crocina KACC 14,589T, D. riboflavina KACC 11,387T and D. salina (Fig. S1). The 16 S rRNA gene phylogenetic trees obtained by the ML and MP algorithms consistently showed identical topologies (Fig. S2 and Fig. S3).
Genomic features
The draft genome of strain PTR5T was composed of 13 contigs and the total genome size was 3.69 Mb with a DNA G + C content of 63.7 mol%. The numbers of coding genes and tRNA genes were 3472 and 46, respectively. The assembly process found no evidence for plasmids and the final sequence yielded was deposited in NCBI GenBank under the accession number JACYFU010000000. The ANI value between strain PTR5T and its close relatives calculated by using the EzBioCloud web server were 75.1–78 %, which was far below the 95–96% threshold for the description of novel species (Yoon et al. 2017). The estimated dDDH value of strain PTR5T with its close relatives of genus Devosia were 19–21.1 %, which was far lower than the threshold value of 70 % for the definition of bacterial species (Meier-Kolthoff et al. 2013) (Table 1). In the phylogenomic tree, strain PTR5T formed an independent lineage close to its reference strains which is consistent with other phylogenetic trees (Fig. 1). Since the core gene phylogeny showed that the genus Devosia is polyphyletic, therefore the AAI values between strain PTR5T and type strains of neighboring genera were also calculated. The AAI values were in the range of 60.3–63.9%, which is far below the threshold value for genus delimitation (65%). CheckM results revealed a 98.9% genome completeness and an estimated 0% genome contamination. Clusters of orthologous genes data of the strain PTR5T genome dataset, obtained from eggNOG analysis, denoted that a total of 1075 genes were assigned to 24 functional categories. Among the obtained functional groups, the cluster for [E] (amino acid transport and metabolism; 279), [G] (carbohydrate transport and metabolism; 265), [P] (inorganic ion transport and metabolism; 235), [K] (transcription; 205), [C] (Energy production and conversion; 174), [J] (translation, ribosomal structure and biogenesis; 162 genes), [T] (signal transduction mechanisms; 163), were the most highly represented categories (in descending order). The comparison of clusters of genes between strain PTR5T and its reference strains is provided in Fig. 2.
Genome analysis with antiSMASH revealed six gene clusters namely two homoserine lactone biosynthetic gene cluster, one betalactone biosynthetic gene cluster, one terpene biosynthetic gene cluster, one Type III PKSs (T3PKS) biosynthetic gene cluster and one ectoine biosynthetic gene cluster which was 83% similar to ectoine. Presence of ectoine biosynthetic gene clusters is responsible for halotolerant characteristics of strain PTR5T. Biosynthetic gene clusters that are responsible for different secondary metabolites in strain PTR5T and its reference strains were compared. Genes for terpene and hserlactone (homoserine lactone) were present in all strains. T3PKS gene cluster was only present in strain PTR5T. Genes for ectoine was present in all strains except D. riboflavina KACC 11,387T, D. soli KACC 11,509T. The presence and absence of gene clusters is presented in table S1.
NCBI annotation revealed six proteins for ectoine biosynthesis: ectoine/hydroxyectoine ABC transporter ATP-binding protein EhuA (JACYFU010000004), ectoine/hydroxyectoine ABC transporter permease subunit EhuD (JACYFU010000004), ectoine/hydroxyectoine ABC transporter permease subunit EhuC (JACYFU010000004), ectoine/hydroxyectoine ABC transporter substrate-binding protein EhuB (JACYFU010000004), ectoine hydroxylase (JACYFU010000004) and ectoine synthase (JACYFU010000004). It can be used as a protective agent for enzymes against stress conditions such as heat, cold, and high or low pH (Galinski and Trüper 1994; Kunte et al. 2014). NCBI also revealed two gene clusters for exopolysaccharide: exopolysaccharide biosynthesis polyprenyl glycosylphosphotransferase (JACYFU010000004), exopolysaccharide biosynthesis protein (JACYFU010000001). Eight gene clusters for polysaccharide proteins were also revealed in the genomes of strain PTR5T, namely one polysaccharide biosynthesis C-terminal domain-containing protein (JACYFU010000001), one divergent polysaccharide deacetylase family protein (JACYFU010000003), two polysaccharide deacetylase family protein (JACYFU010000001), one polysaccharide export protein (JACYFU010000001), one polysaccharide biosynthesis/export family protein (JACYFU010000002) and one polysaccharide biosynthesis protein (JACYFU010000002) (Table S1). PTR5T produces sufficient amount of extracellular polymeric substances (EPS) on agar plates, the presence of genes and the phenotypic results were consistent with each other. Gene clusters for siderophore biosynthesis, auxin response and tryptophan biosynthesis were annotated in the genome strain PTR5T and its reference strains. The number of genes for auxin response and tryptophan biosynthesis were almost same in all species however number of gene clusters for siderophore biosynthesis were vary in all strains. Interestingly, the novel strain PTR5T contain less number of genes for siderophore as compared to other close relatives. Among all species, D. crocina KACC 14,589T and D. riboflavina KACC 11,387T had the highest number of genes for siderophore. Genes related to nitrogen fixation were not found. Presence of genes responsible for IAA and siderophore biosynthesis among strains is provided in Table S1. Candidate genes involved in resistance to antibiotics and toxic compounds were also investigated using RAST Server. In strain PTR5T, 39 gene clusters were found including: copper homeostasis (16), cobalt-zinc-cadmium resistance (11), mercuric reductase (1), tetracycline resistance, ribosome protection type (4), copper tolerance (3), resistance to fluoroquinolones (2), beta-lactamase (1) and resistance to chromium compounds (1). Its reference strains also contains genes involved in resistance to antibiotics and toxic compounds, the comparison of number of genes is presented in table S2. The heavy metals As, Au, Zn, Cd, Ur, Se, Ag, Hg, Cr and Ni are hazardous heavy metals that contaminate the environment and adversely affects the quality of the soil, crop production as well as public health (Kuhlmann et al. 2011; Ndeddy Aka et al. 2016; Glick 1995). The application of strain PTR5T, as bioremediation of heavy metals and antibiotics contaminated soils can enhance plant growth against heavy metal toxicity and increase heavy metal removal efficiency.
Physiology and chemotaxonomy
Cells of strain PTR5T were Gram-reaction-negative, motile, aerobic, non-spore-forming and long-rods. Morphology of cells of strain PTR5T is available as Fig. 3. Colonies were white-pigmented, and smooth and watery after incubation for 3 days on R2A agar. Strain PTR5T could grow on R2A, LB, NA, MA and TSA agar. Growth occured at 5–38 °C (optimum, 30 °C), pH 4.0–8.0 (optimum, pH 7.0) and 0–10 % (w/v) NaCl (optimum, 0 %). Cell growth was not found in the addition of 10.5% NaCl. PTR5T produces sufficient amount of EPS on agar plates. EPS provide a microenvironment that holds water and dries more slowly compared with the surrounding environment, thus protecting bacteria and roots of plants against desiccation (Sandhya et al. 2009). The hydrolysis of urease, esculin, casein, CM-cellulose, starch and chitin does not occur while that of gelatin occurs. Other reference strains did not produced EPS in agar plates which differentiates the strain PTR5T visually from its close relatives. Absence of pigmentation in colonies of strain PTR5T differentiates it with its most close relatives. Moreover, the higher NaCl tolerance ability of strain PTR5T differentiates it from its reference strains. Other phenotypic features of strain PTR5T were summarized in the species description and properties differentiating the isolate from type strains of closely related species were detailed in Table 2.
The major fatty acids (> 10 % of the total fatty acids) detected in strain PTR5T were C16:0, C18:1 ω7c 11-methyl and summed feature 8 (comprising C18:1 ω7c/C18:1 ω6c) in line with the reference strains. The little percentage of C11:0 and absence of C16:0 in strain PTR5T differentiate it from other close relatives. Differences between strain PTR5T and the reference strains were detailed in Table S3. The predominant respiratory quinone detected in strain PTR5T was ubiquinone Q-10 and the major polar lipids were phosphatidylglycerol (PG), diphosphatidylglycerol (DPG), one unidentified phosphoglycolipid (PGL), two unidentified aminolipids (AL1-2), three unidentified aminoglycolipids (AGL1-3), two unidentified glycolipids (GL1-2) and two unidentified lipids (L1-2), which were consistent with other members of the genus Devosia (Fig. S4).
Plant growth promoting traits
Strains PTR5T showed the ability to synthesize IAA in the presence of the precursor l-tryptophan and could produce 19.4 µg/ml IAA (Fig. S6). Growth of strain PTR5T was not observed in Jensen’s nitrogen free medium which confirm that this novel strain is not able to fix nitrogen like most species of Devosia. Strain PTR5T was also able to produce siderophores, as this was confirmed by the production of uncolored halos around colonies on CAS agar which is blue in color (not shown).
Description of Devosia oryzisoli sp. nov.
Devosia oryzisoli (o.ry.zi.so′li. L. fem. n. oryza rice; L. gen. n. soli of the soil; N.L. gen. n. oryzisoli of the rice root).
Cells are Gram-stain negative, aerobic, flagellated and rod-shaped. Colonies are smooth, convex, opaque, circular with regular margins, white in color, and 1–3 mm in diameter and produce slime materials after 3 days of incubation at 30 °C. Growth occurs at 5–38 °C (optimum, 30 °C), pH 4.0–8.0 (optimum, 7.0) and in the presence of 0–10% (w/v) NaCl (optimum, 0%). Cells do not produce carotenoid and flexirubin-type pigments. Cells grew well on R2A and LB and moderately on TSA, NA and MA. Cells are positive for catalase and oxidase activities. The hydrolysis of urease, esculin, casein, CM-cellulose, starch and chitin does not occur while that of gelatin occurs. In API 20NE, strain showed positive results for indole production, glucose fermentation and arginine dihydrolase production. The assimilation of L-arabinose, D-mannose, D-mannitol, D-maltose and potassium gluconate occurs In API ZYM, cells are positive for alkaline phosphatase, esterase, esterase lipase, leucine arylamidase, valline arylamidase, naphtol-AS-BI-phosphohydrolase, β-galactosidase, α-glucosidase, β-glucosidase and N-acetyl-β-glucosaminidase. The major fatty acids are C16:0, C18:1 ω7c 11-methyl and summed feature 8 (comprising C18:1 ω7c/C18:1 ω6c). Q-10 is the predominant respiratory quinone and the polar lipids are phosphatidylglycerol, diphosphatidylglycerol, one unidentified phosphoglycolipid, three unidentified aminoglycolipids, two unidentified aminolipids, two unidentified glycolipids and two unidentified lipids.
The type strain, isolated from roots of rice plants collected from a paddy field in Ilsan, Republic of Korea, is PTR5T (= KCTC 82691T = TBRC 15163T). The DNA G + C content of the strain is 63.7%. The GenBank/EMBL/DDBJ/PIR accession number for the 16 S rRNA gene sequence of strain PTR5T is OP763491. The NCBI accession number for the whole genome sequence of strain PTR5T is JACYFU000000000.
Abbreviations
- ANI:
-
Average nucleotide identity
- dDDH:
-
Digital DNA–DNA hybridization
- AAI:
-
Amino acid identity
- PGP:
-
Plant growth-promoting
- IAA:
-
Indole acetic acid
- KCTC:
-
Korean Collection for Type Cultures
- TBRC:
-
Thailand Bioresource Research Center
- EPS:
-
Extracellular polymeric substance
- CAS:
-
Chrome Azurol S
References
Aziz RK, Bartels D, Best AA, DeJongh M, Disz T et al (2008) The RAST server: rapid annotations using subsystems technology. BMC Genomics 9:75. https://doi.org/10.1186/1471-2164-9-75
Blin K, Shaw S, Villebro SK, Zeimert NR, Lee SY, Medema M, Weber T (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87. https://doi.org/10.1093/nar/gkz310
Chhetri G, Kim J, Kim I, Kim H, Seo T (2020) Hymenobacter setariae sp. nov., isolated from the ubiquitous weedy grass Setaria viridis. Int J Syst Evol Microbiol 70:3724–3730. https://doi.org/10.1099/ijsem.0.004226
Chhetri G, Kim I, Kang M et al (2022) Devosia rhizoryzae sp. nov., and Devosia oryziradicis sp. nov., novel plant growth promoting members of the genus Devosia, isolated from the rhizosphere of rice plants. J Microbiol 60:1–10. https://doi.org/10.1007/s12275-022-1474-8
Collins MD, Jones D (1981) Distribution of isoprenoid quinone structural types in bacteria and their taxonomic implications. Microbiol Rev 45:316–354. https://doi.org/10.1128/mr.45.2.316-354.1981
Dua A, Malhotra J, Saxena A, Khan F, Lal R (2013) Devosia lucknowensis sp. nov., a bacterium isolated from hexachlorocyclohexane (HCH) contaminated pond soil. J Microbiol 51:689–694. https://doi.org/10.1007/s12275-013-2705-9
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376. https://doi.org/10.1007/BF01734359
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678
Fitch WM (1971) Toward defining the course of evolution: minimum change for a specific tree topology. Syst Zool 20:406–416. https://doi.org/10.1093/sysbio/20.4.406
Galatis H, Martin K, Kämpfer P, Glaeser SP (2013) Devosia epidermidihirudinis sp. nov. isolated from the surface of a medical leech. Antonie Van Leeuwenhoek 103:1165–1171. https://doi.org/10.1007/s10482-013-9895-3
Galinski EA, Trüper HG (1994) Microbial behaviour in salt-stressed ecosystems. FEMS Microbiol Rev 15:95–108. https://doi.org/10.1111/j.1574-6976.1994.tb00128.x
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:09–117. https://doi.org/10.1139/m95-015
Huerta-Cepas J, Szklarczyk D, Forslund K, Cook H, Heller D et al (2016) eggNOG 4.5: a hierarchical orthology framework with improved functional annotations for eukaryotic, prokaryotic and viral sequences. Nucleic Acids Res 44:D286–D293. https://doi.org/10.1093/nar/gkv1248
Jia YY, Sun C, Pan J, Zhang WY, Zhang X-Q et al (2014) Devosia pacifica sp. nov., isolated from deep-sea sediment. Int J Syst Evol Microbiol 64:2637–2641. https://doi.org/10.1099/ijs.0.059626-0
Kang M, Chhetri G, Kim J, Kim I, Seo T (2021) Sphingomonas sabuli sp. nov., a carotenoid-producing bacterium isolated from beach sand. Int J Syst Evol Microbiol 71:004896. https://doi.org/10.1099/ijsem.0.004896
Kim I, Chhetri G, Kim J, Seo T (2019a) Amnibacterium setariae sp. nov., an endophytic actinobacterium isolated from dried foxtail. Antonie Van Leeuwenhoek 112:1731–1738. https://doi.org/10.1007/s10482-019-01302-7
Kim I, Kim J, Chhetri G, Seo T (2019b) Flavobacterium humi sp. nov., a flexirubin-type pigment producing bacterium, isolated from soil. J Microbiol 57:1079–1085. https://doi.org/10.1007/s12275-019-9350-x
Kim J, Chhetri G, Kim I et al (2020) Methylobacterium terrae sp. nov., a radiation-resistant bacterium isolated from gamma ray-irradiated soil. J Microbiol 959:966. https://doi.org/10.1007/s12275-019-9007-9
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. doi: https://doi.org/10.1007/BF01731581
Komagata K, Suzuki KI (1987) Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol 19:161205. https://doi.org/10.1016/S0580-9517(08)70410-0
Kuhlmann AU, Hoffmann T, Bursy J, Jebbar M, Bremer E (2011) Ectoine and hydroxyectoine as protectants against osmotic and cold stress: uptake through the SigB-controlled betaine–choline–carnitine transporter-type carrier EctT from Virgibacillus pantothenticus. J Bacteriol 193(18):4699–4708. https://doi.org/10.1128/JB.05270-11
Kumar S, Stecher G, Tamura K (2016) Mega7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Kunte HJ, Lentzen G, Galinski E (2014) Industrial production of the cell protectant ectoine: protection, mechanisms, processes, and products. Curr Biotechnol 66:10–25. https://doi.org/10.2174/22115501113026660037
Kuykendall LD, Roy MA, O’Neill JJ, Devine TE (1988) Fatty acids, antibiotic resistance and deoxyribonucleic acid homology groups of Bradyrhizobium japonicum. Int J Syst Evol Microbiol 38:358–361. https://doi.org/10.1099/00207713-38-4-358
Lee SD (2007) Devosia subaequoris sp. nov., isolated from beach sediment. Int J Syst Evol Microbiol 57:2212–2215. https://doi.org/10.1099/ijs.0.65185-0
Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M (2013) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinform 14:60. https://doi.org/10.1186/1471-2105-14-60
Minnikin DE, O’Donnell AG, Goodfellow M, Alderson G, Athalye M et al (1984) An integrated procedure for the extraction of bacterial isoprenoid quinones and polar lipids. J Microbiol Methods 2:233–241. https://doi.org/10.1016/0167-7012(84)90018-6
Na SI, Kim YO, Yoon SH, Ha SM, Baek I et al (2018) UBCG: up-to-date bacterial core gene set and pipeline for phylogenomic tree reconstruction. J Microbiol 56:280–285. https://doi.org/10.1007/s12275-018-8014-6
Nakagawa Y, Sakane T, Yokota A (1996) Transfer of “Pseudomonas riboflavina” (Foster 1944), a gram-negative, motile rod with long-chain 3-hydroxy fatty acids, to Devosia riboflavina gen. nov., sp. nov., nom. rev. Int J Syst Bacteriol 46:16–22. https://doi.org/10.1099/00207713-46-1-16
Ndeddy Aka RJ, Babalola OO (2016) Effect of bacterial inoculation of strains of pseudomonas aeruginosa, alcaligenes feacalis and Bacillus subtilis on germination, growth and heavy metal (cd, cr, and Ni) uptake of Brassica juncea. Int J Phytorem 18:200–209. DOI: https://doi.org/10.1080/15226514.2015.1073671
Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW (2015) CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 25:1043–1055. https://doi.org/10.1101/gr.186072.114
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sandhya V, Ali SKZ, Grover M, Reddy G, Venkateswarlu B (2009) Alleviation of drought stress effects in sunflower seedlings by the exopolysaccharides producing Pseudomonas putida strain GAP-P45. Biol Fertil Soils 46:17–26. https://doi.org/10.1007/s00374-009-0401-z
Sato I, Ito M, Ishizaka M, Ikunaga Y, Sato Y, Yoshida S, Koitabashi M, Tsushima S (2012) Thirteen novel deoxynivalenoldegrading bacteria are classified within two genera with distinct degradation mechanisms. FEMS Microbiol Lett 327:110–117. https://doi.org/10.1111/j.1574-6968.2011.02461.x
Smibert RM, Krieg NR (1994) Phenotypic characterization. In: Gerhardt P, Murray RGE, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington, DC, pp 607–654
So Y, Chhetri G, Kim I, Kang M, Kim J, Lee B, Jang W, Seo T (2022) Halomonas antri sp. nov., a carotenoid-producing bacterium isolated from surface seawater. Int J Syst Evol Microbiol 72:005272. https://doi.org/10.1099/ijsem.0.005272
Tatusova T, DiCuccio M, Badretdin A, Chetvernin V, Nawrocki EP et al (2016) NCBI prokaryotic genome annotation pipeline. Nucleic Acids Res 44:6614–6624. https://doi.org/10.1093/nar/gkw569
Thompson J, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. https://doi.org/10.1093/nar/25.24.4876
Vanparys B, Heylen K, Lebbe L, De Vos P (2005) Devosia limi sp. nov., isolated from a nitrifying inoculum. Int J Syst Evol Microbiol 55:1997–2000. https://doi.org/10.1099/ijs.0.63714-0
Wang G, Wang Y, Ji F, Xu L, Yu M, Shi J, Xu J (2019) Biodegradation of deoxynivalenol and its derivatives by Devosia insulae A16. Food Chem 276:436–442. https://doi.org/10.1016/j.foodchem.2018.10.011
Yoon JH, Kang SJ, Park S, Oh TK (2007) Devosia insulae sp. nov., isolated from soil, and emended description of the genus Devosia. Int J Syst Evol Microbiol 57:1310–1314. https://doi.org/10.1099/ijs.0.65028-0
Yoon SH, Ha SM, Lim J, Kwon S, Chun J (2017) A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie Van Leeuwenhoek 110:1281–1286. https://doi.org/10.1007/s10482-017-0844-4
Zhang DC, Redzic M, Liu HC, Zhou YG, Schinner F et al (2012) Devosia psychrophila sp. nov. and Devosia glacialis sp. nov., from alpine glacier cryoconite, and an emended description of the genus Devosia. Int J Syst Evol Microbiol 62:710–715. https://doi.org/10.1099/ijs.0.023937-0
Acknowledgements
We thank Prof Dr. Bernhard Schink (University of Konstanz, Konstanz, Germany) for the suggestion about species epithet.
Funding
This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR202102205), and by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2022R1F1A107108).
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Chhetri, G., Kim, I. & Seo, T. Devosia oryzisoli sp. nov., a novel moderately halotolerant bacterium isolated from the roots of rice plants and genome mining revealed the biosynthesis potential as plant growth promoter. Antonie van Leeuwenhoek 116, 231–242 (2023). https://doi.org/10.1007/s10482-022-01800-1
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DOI: https://doi.org/10.1007/s10482-022-01800-1