Stimulation of Nicotiana tabacum L. In Vitro Shoot Growth by Endophytic Bacillus cereus Group Bacteria
Abstract
:1. Introduction
2. Materials and Methods
2.1. Isolation of Cultivable Endophytic Bacteria
2.2. Identification of Bacterial Isolates and Bacterial Genome Analysis
2.3. Bacterial Genome Sequencing, Annotation and Comparative Analysis
2.4. Tobacco In Vitro Shoot Co-Cultivation with Endophytic Bacteria
2.5. Analysis of Endophytic Bacteria Density in Tobacco Shoot Tissues
3. Results
3.1. Isolation and Identification of Cultivable Endophytic Bacteria
3.2. Endophytic Bacteria Co-Cultivation Effect on Tobacco Shoot Biomass Accumulation
3.3. Survival of Endophytic Bacteria Isolates in Tobacco Shoot Tissues
3.4. Comparative Genome Analysis of Closely Related B. toyonensis Isolates
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Appendix A
Clade No. a | Bacterial Strain | Accession b | Accession Length, bp | Sequence Identity, % | Reference |
---|---|---|---|---|---|
1 A | Bacillus thuringiensis IAM 12077 | NR_043403.1 | 1486 | 97.3–99.9 | [106] |
1 B | Bacillus mobilis MCCC 1A05942 | NR_157731.1 | 1509 | 97.1–99.8 | [107] |
1 C | Bacillus mycoides DSM 11821 | NR_024697.1 | 1531 | 97.8–100.0 | [108] |
2 | Bacillus marisflavi TF-11 | NR_025240.1 | 1506 | 98.1–98.9 | [109] |
3 | Bacillus simplex NBRC 15720 = DSM 1321 | NR_112726.1 | 1476 | 95.4–99.7 | d.s. |
4 | Bacillus aryabhattai B8W22 | NR_115953.1 | 1533 | 95.0–97.5 | [110] |
5 | Bacillus pumilus NBRC 12092 | NR_112637.1 | 1474 | 99.89 | d.s. |
6 | Pseudomonas koreensis Ps 9-14 | NR_025228.1 | 1455 | 99.5 | [111] |
Parameter | Isolate | ||
---|---|---|---|
Nt.18 | Nt.37 | Nt.3.2 | |
Illumina demultiplexing and read mapping statistics | |||
Number of read pairs | 2,468,194 | 2,298,751 | 2,950,725 |
Yield (mbp) | 666 | 596 | 797 |
Average quality | 36.03 | 36.23 | 36.14 |
Total reads | 4,936,388 | 4,597,502 | 5,901,450 |
Mapped reads | 4,899,758 | 4,571,302 | 5,869,378 |
Average coverage | 119.6 | 107.16 | 135.82 |
Insert size median | 317 | 272 | 300 |
De novo short-read assembly statistics | |||
Genome Length (bp) | 5,574,424 | 5,586,422 | 5,891,672 |
GC Content (%) | 35.0626 | 35.090523 | 34.933907 |
Contigs N50 (bp) | 564,507 | 276,397 | 324,644 |
Number of scaffolds | 52 | 90 | 91 |
Average scaffold size (bp) | 107,200 | 62,071 | 64,743 |
Max scaffold size (bp) | 1,307,898 | 934,026 | 1,427,494 |
Min scaffold size (bp) | 311 | 587 | 335 |
Number of gaps | 3 | 5 | 5 |
Genome quality statistics | |||
Completeness (%) | 99.34 | 99.43 | 99.34 |
Contamination (%) | 0.23 | 0.11 | 0.1 |
Closest placement taxonomic assignment | |||
Species | Bacillus toyonensis | Bacillus toyonensis | Bacillus wiedmannii |
GTDB species representative | BCT-7112 | BCT-7112 | FSL W8-0169 |
GTDB reference | GCF_000496285.1 | GCF_000496285.1 | GCF_001583695.1 |
TYGS accession | NCIMB 14858 | NCIMB 14858 | FSL W8-0169 |
ANI (%) | 99.39 | 99.33 | 96.49 |
Alignment fraction (%) | 0.95 | 0.95 | 0.91 |
Annotation statistics | |||
Features | 5853 | 5905 | 6424 |
Coding gene | 5761 | 5814 | 6217 |
RNAs | 92 | 91 | 96 |
Distinct functions | 4049 | 4072 | 4136 |
Non-hypothetical proteins | 3707 | 3729 | 3933 |
Hypothetical proteins | 2054 | 2085 | 2284 |
Query | Reference | ANI Estimate | Matches | Total |
---|---|---|---|---|
Nt.18 | Nt.37 | 99.554 | 1740 | 1833 |
Nt.37 | Nt.18 | 99.482 | 1746 | 1814 |
Nt.18 | Nt.3.2 | 91.356 | 1527 | 1833 |
Nt.37 | Nt.3.2 | 91.328 | 1529 | 1814 |
Nt.3.2 | Nt.18 | 91.242 | 1553 | 1923 |
Nt.3.2 | Nt.37 | 91.222 | 1528 | 1923 |
Parameter | Isolate | |
---|---|---|
Nt.18 | Nt.37 | |
Annotation statistics | ||
Features | 5853 | 5905 |
Coding gene | 5761 | 5814 |
RNAs | 92 | 91 |
Distinct functions | 4049 | 4072 |
Non-hypothetical proteins | 3707 | 3729 |
Hypothetical proteins | 2054 | 2085 |
Comparative analysis statistics | ||
Genes in core homolog families | 5576 | 5594 |
Genes in singletons | 185 (60) a | 220 (20) a |
Genes with ≥90% identity | 5425 | |
Genes with <90% identity | 151 (52) a |
Symbol | Genome Feature No. | Gene Name | Id., % | Pfam | |||
---|---|---|---|---|---|---|---|
Nt.18 | Nt.37 | Domain | Reference | E Value | |||
Cluster number 36; Cluster type LAP | |||||||
Core biosynthetic genes | |||||||
HP | 5593 | Hypothetical protein | YcaO | PF02624.16 | 4 × 10−58 | ||
HP | 5594 | Hypothetical protein | Nitroreductase | PF00881.24 | 5.3 × 10−11 | ||
Cluster number 20; Cluster Type: saccharide, EPS related cluster | |||||||
Core biosynthetic genes | |||||||
UDPGE | 3491 | 2631 | UDP-glucose 4-epimerase (EC 5.1.3.2) | 100 | Epimerase | PF01370.21 | 1.5 × 10−57 |
MAEP | 3503 | Multi antimicrobial extrusion protein (Na(+)/drug antiporter), MATE family of MDR efflux pumps | Polysacc synt Polysacc synt C | PF01943.17 PF14667.6 | 9.6 × 10−16 2 × 10−9 | ||
HP | 3506 | Hypothetical protein | Glycos transf 1 Glyco transf 4 | PF00534.20 PF13439.6 | 9.1 × 10−28 8.6 × 10−9 | ||
UFS | 3508 | UDP-N-acetyl-L-fucosamine synthase (EC 5.1.3.28) | Epimerase 2 | PF02350.19 | 1.9 × 10−88 | ||
CPBP | 3509 | Capsular polysaccharide synthesis enzyme Cap5F | Epimerase GPI | PF01370.21 PF06560.11 | 4.4 × 10−20 4.7 × 10−5 | ||
UGADH | 3510 | UDP-N-acetylglucosamine 4,6-dehydratase (EC 4.2.1.135) | Polysacc synt 2 Polysacc syn 2C | PF02719.15 PF08485.10 | 3 × 10−103 9.2 × 10−23 | ||
CPBP | 3511 | Capsular polysaccharide biosynthesis protein Cps4F | Glycos transf 1 Glyco trans 4 4 | PF00534.20 PF13579.6 | 3.2 × 10−18 5.4 × 10−13 | ||
UPGPT | 3512 | 2613 | Undecaprenyl-phosphate galactosephosphotransferase (EC2.7.8.6) | 40 | Bac transf | PF02397.16 | 2.1 × 10−62 |
PPBP | 3513 | Probable polysaccharide biosynthesis protein EpsC | Polysacc synt 2 CoA binding 3 | PF02719.15 PF13727.6 | 7 × 10−124 6 × 10−20 | ||
UGP | 3514 | 2612 | UTP--glucose-1-phosphate uridylyltransferase (EC 2.7.7.9) | 96 | NTP transferase | PF00483.23 | 2.2 × 10−35 |
HP | 2615 | hypothetical protein | 19 | Glycos transf 1 | PF00534.20 | 2.1 × 10−13 | |
HP | 2616 | Hypothetical protein | Polysacc synt | PF01943.17 | 4.5 × 10−15 | ||
GTF | 2620 | Glycosyltransferase | 22 | Glyco trans 1 4 | PF13692.6 | 3 × 10−13 | |
EPGTF | 2621 | Exopolysaccharide biosynthesis glycosyltransferase EpsF (EC 2.4.1.) | Glyco transf 4 Glycos transf 1 | PF13439.6 PF00534.20 | 1.4 × 10−19 1.6 × 10−24 | ||
GTF | 2622 | Glycosyltransferase | Glyco transf 4 Glycos transf 1 | PF13439.6 PF00534.20 | 1.3 × 10−8 3.2 × 10−26 | ||
SPGT | 2623 | Sugar-phosphate guanylyltransferase/Sugar-phosephate isomerase | NTP transferase MannoseP isomer | PF00483.23 PF01050.18 | 2 × 10−32 2.3 × 10−19 | ||
Additional biosynthetic and transport-related genes | |||||||
CPCT | 3494 | 2628 | Choline-phosphate cytidylyltransferase (EC 2.7.7.15)/Choline kinase (EC 2.7.1.32) | 99 | HTH 24 NTP transf 3 Choline kinase | PF13412.6 PF12804.7 PF01633.20 | 1.3 × 10−11 3.5 × 10−9 9.5 × 10−34 |
UMDH | 2614 | UDP-N-acetyl-D-mannosamine dehydrogenase (EC 1.1.1.336) | UDPG MGDP dh N UDPG MGDP dh UDPG MGDP dh C | PF03721.14 PF00984.19 PF03720.15 | 5 × 10−58 5.8 × 10−28 8.1 × 10−20 | ||
HP | 2618 | Hypothetical protein | Acyl transf 3 | PF01757.22 | 1.3 × 10−31 | ||
HP | 3493 | 2629 | Hypothetical protein | 100 | EamA | PF00892.20 | 9.3 × 10−12 |
Other genes | |||||||
HP | 3507 | Hypothetical protein | |||||
HP | 3505 | Hypothetical protein | O-ag pol Wzy | PF14296.6 | 4.7 × 10−23 | ||
HP | 3504 | Hypothetical protein | MAF flag10 | PF01973.18 | 6.7 × 10−14 | ||
KDSB | 3502 | 3-deoxy-manno-octulosonate cytidylyltransferase (EC 2.7.7.38) | CTP transf 3 | PF02348.19 | 2.9 × 10−55 | ||
KDOPS | 3501 | 2-Keto-3-deoxy-D-manno-octulosonate-8-phosphate synthase (EC 2.5.1.55) | DAHP synth 1 | PF00793.20 | 1 × 10−71 | ||
API | 3500 | D-arabinose-5-phosphate isomerase (EC 5.3.1.13) | SIS CBS | PF01380.22 PF00571.28 | 1.1 × 10−28 1.3 × 10−8 | ||
KDOPP | 3499 | 3-deoxy-D-manno-octulosonate 8-phosphate phosphatase (EC 3.1.3.45) | Hydrolase 3 | PF08282.12 | 2.6 × 10−9 | ||
HP | 3498 | Hypothetical protein | HIT | PF01230.23 | 3.1 × 10−7 | ||
LCP | 3497 | 2625 | Cell envelope-associated transcriptional attenuator LytR-CpsA-Psr, subfamily F2 | 75 | LytR cpsA psr | PF03816.14 | 2 × 10−50 |
EPSX | 3496 | 2626 | EPSX protein | 99 | |||
HP | 3495 | 2627 | Hypothetical protein | 100 | LicD | PF04991.13 | 3.5 × 10−6 |
CPCT | 3492 | 2630 | Choline-phosphate cytidylyltransferase (EC 2.7.7.15) | 98 | NTP transferase | PF00483.23 | 1.8 × 10−12 |
HP | 2617 | Hypothetical protein | Hepar II III N Hepar II III | PF16889.5 PF07940.13 | 3.2 × 10−16 5.4 × 10−21 | ||
HP | 2619 | Hypothetical protein | |||||
CPCT | 2624 | Mannose-6-phosphate isomerase (EC 5.3.1.8) | PMI typeI | PF01238.21 | 5.8 × 10−47 |
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Andriūnaitė, E.; Tamošiūnė, I.; Aleksandravičiūtė, M.; Gelvonauskienė, D.; Vinskienė, J.; Rugienius, R.; Baniulis, D. Stimulation of Nicotiana tabacum L. In Vitro Shoot Growth by Endophytic Bacillus cereus Group Bacteria. Microorganisms 2021, 9, 1893. https://doi.org/10.3390/microorganisms9091893
Andriūnaitė E, Tamošiūnė I, Aleksandravičiūtė M, Gelvonauskienė D, Vinskienė J, Rugienius R, Baniulis D. Stimulation of Nicotiana tabacum L. In Vitro Shoot Growth by Endophytic Bacillus cereus Group Bacteria. Microorganisms. 2021; 9(9):1893. https://doi.org/10.3390/microorganisms9091893
Chicago/Turabian StyleAndriūnaitė, Elena, Inga Tamošiūnė, Monika Aleksandravičiūtė, Dalia Gelvonauskienė, Jurgita Vinskienė, Rytis Rugienius, and Danas Baniulis. 2021. "Stimulation of Nicotiana tabacum L. In Vitro Shoot Growth by Endophytic Bacillus cereus Group Bacteria" Microorganisms 9, no. 9: 1893. https://doi.org/10.3390/microorganisms9091893