Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants
IntroductionEndophytes are colonizers of healthy plants and they normally exhibit biocontrol activities, such as reducing the occurrence of plant diseases and promoting plant growth. The endophytic bacterium Bacillus halotolerans Q2H2 (Q2H2) was isolated from the roots of potato plants and was found...
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Frontiers Media S.A.
2024-01-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1287921/full |
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| author | Yuhu Wang Zhenqi Sun Qianqian Zhao Xiangdong Yang Yahui Li Hongyou Zhou Mingmin Zhao Hongli Zheng |
| author_facet | Yuhu Wang Zhenqi Sun Qianqian Zhao Xiangdong Yang Yahui Li Hongyou Zhou Mingmin Zhao Hongli Zheng |
| author_sort | Yuhu Wang |
| collection | DOAJ |
| description | IntroductionEndophytes are colonizers of healthy plants and they normally exhibit biocontrol activities, such as reducing the occurrence of plant diseases and promoting plant growth. The endophytic bacterium Bacillus halotolerans Q2H2 (Q2H2) was isolated from the roots of potato plants and was found to have an antagonistic effect on pathogenic fungi.MethodsQ2H2 was identified by morphological observations, physiological and biochemical identification, and 16S rRNA gene sequence analysis. Genes related to the anti-fungal and growth-promoting effects were analyzed using whole-genome sequencing and comparative genomic analysis. Finally, we analyzed the growth-promoting and biocontrol activities of Q2H2 in potato plants using pot experiments.ResultsAntagonism and non-volatile substance plate tests showed that Q2H2 had strong antagonism against Fusarium oxysporum, Fusarium commune, Fusarium graminearum, Fusarium brachygibbosum, Rhizoctonia solani and Stemphylium solani. The plate test showed that Q2H2 had the ability to produce proteases, cellulases, β-1,3-glucanase, dissolved organic phosphate, siderophores, indole-3-acetic acid (IAA), ammonia and fix nitrogen. The suitable growth ranges of Q2H2 under different forms of abiotic stress were pH 5–9, a temperature of 15–30°C, and a salt concentration of 1–5%. Though whole-genome sequencing, we obtained sequencing data of approximately 4.16 MB encompassed 4,102 coding sequences. We predicted 10 secondary metabolite gene clusters related to antagonism and growth promotion, including five known products surfactin, bacillaene, fengycin, bacilysin, bacillibactin, and subtilosin A. Average nucleotide identity and comparative genomic analyses revealed that Q2H2 was Bacillus halotolerans. Through gene function annotation, we analyzed genes related to antagonism and plant growth promotion in the Q2H2 genome. These included genes involved in phosphate metabolism (pstB, pstA, pstC, and pstS), nitrogen fixation (nifS, nifU, salA, and sufU), ammonia production (gudB, rocG, nasD, and nasE), siderophore production (fhuC, fhuG, fhuB, and fhuD), IAA production (trpABFCDE), biofilm formation (tasA, bslA, and bslB), and volatile compound production (alsD, ilvABCDEHKY, metH, and ispE), and genes encoding hydrolases (eglS, amyE, gmuD, ganB, sleL, and ydhD). The potato pot test showed that Q2H2 had an obvious growth-promoting effect on potato roots and better control of Fusarium wilt than carbendazim.ConclusionThese findings suggest that the strain-specific genes identified in bacterial endophytes may reveal important antagonistic and plant growth-promoting mechanisms. |
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| spelling | doaj.art-14b4b9556b4e4beaaa13226d2fb110a32024-01-03T04:12:42ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2024-01-011410.3389/fmicb.2023.12879211287921Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plantsYuhu Wang0Zhenqi Sun1Qianqian Zhao2Xiangdong Yang3Yahui Li4Hongyou Zhou5Mingmin Zhao6Hongli Zheng7College of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaCollege of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaInstitute of Agro-Food Technology, Jilin Academy of Agricultural Sciences, Changchun, ChinaJilin Provincial Key Laboratory of Agricultural Biotechnology, Jilin Academy of Agricultural Sciences, Changchun, ChinaCollege of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaCollege of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaCollege of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaCollege of Horticulture and Plant Protection, Inner Mongolia Agricultural University, Hohhot, ChinaIntroductionEndophytes are colonizers of healthy plants and they normally exhibit biocontrol activities, such as reducing the occurrence of plant diseases and promoting plant growth. The endophytic bacterium Bacillus halotolerans Q2H2 (Q2H2) was isolated from the roots of potato plants and was found to have an antagonistic effect on pathogenic fungi.MethodsQ2H2 was identified by morphological observations, physiological and biochemical identification, and 16S rRNA gene sequence analysis. Genes related to the anti-fungal and growth-promoting effects were analyzed using whole-genome sequencing and comparative genomic analysis. Finally, we analyzed the growth-promoting and biocontrol activities of Q2H2 in potato plants using pot experiments.ResultsAntagonism and non-volatile substance plate tests showed that Q2H2 had strong antagonism against Fusarium oxysporum, Fusarium commune, Fusarium graminearum, Fusarium brachygibbosum, Rhizoctonia solani and Stemphylium solani. The plate test showed that Q2H2 had the ability to produce proteases, cellulases, β-1,3-glucanase, dissolved organic phosphate, siderophores, indole-3-acetic acid (IAA), ammonia and fix nitrogen. The suitable growth ranges of Q2H2 under different forms of abiotic stress were pH 5–9, a temperature of 15–30°C, and a salt concentration of 1–5%. Though whole-genome sequencing, we obtained sequencing data of approximately 4.16 MB encompassed 4,102 coding sequences. We predicted 10 secondary metabolite gene clusters related to antagonism and growth promotion, including five known products surfactin, bacillaene, fengycin, bacilysin, bacillibactin, and subtilosin A. Average nucleotide identity and comparative genomic analyses revealed that Q2H2 was Bacillus halotolerans. Through gene function annotation, we analyzed genes related to antagonism and plant growth promotion in the Q2H2 genome. These included genes involved in phosphate metabolism (pstB, pstA, pstC, and pstS), nitrogen fixation (nifS, nifU, salA, and sufU), ammonia production (gudB, rocG, nasD, and nasE), siderophore production (fhuC, fhuG, fhuB, and fhuD), IAA production (trpABFCDE), biofilm formation (tasA, bslA, and bslB), and volatile compound production (alsD, ilvABCDEHKY, metH, and ispE), and genes encoding hydrolases (eglS, amyE, gmuD, ganB, sleL, and ydhD). The potato pot test showed that Q2H2 had an obvious growth-promoting effect on potato roots and better control of Fusarium wilt than carbendazim.ConclusionThese findings suggest that the strain-specific genes identified in bacterial endophytes may reveal important antagonistic and plant growth-promoting mechanisms.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1287921/fullbacterial endophytesBacillus halotoleransplant growth-promotingantagonistic activitiesbiological controlwhole-genome sequencing |
| spellingShingle | Yuhu Wang Zhenqi Sun Qianqian Zhao Xiangdong Yang Yahui Li Hongyou Zhou Mingmin Zhao Hongli Zheng Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants Frontiers in Microbiology bacterial endophytes Bacillus halotolerans plant growth-promoting antagonistic activities biological control whole-genome sequencing |
| title | Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants |
| title_full | Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants |
| title_fullStr | Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants |
| title_full_unstemmed | Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants |
| title_short | Whole-genome analysis revealed the growth-promoting and biological control mechanism of the endophytic bacterial strain Bacillus halotolerans Q2H2, with strong antagonistic activity in potato plants |
| title_sort | whole genome analysis revealed the growth promoting and biological control mechanism of the endophytic bacterial strain bacillus halotolerans q2h2 with strong antagonistic activity in potato plants |
| topic | bacterial endophytes Bacillus halotolerans plant growth-promoting antagonistic activities biological control whole-genome sequencing |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1287921/full |
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