Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta
Citrus huanglongbing (HLB) is a devastating disease for the citrus industry. The previous studies demonstrated that oxytetracycline and penicillin are effective antibiotics against <i>Candidatus</i> Liberibacter asiaticus (<i>C</i>Las). However, since <i>C</i>Las...
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MDPI AG
2020-12-01
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| Series: | Antibiotics |
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| Online Access: | https://www.mdpi.com/2079-6382/9/12/874 |
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| author | Chuanyu Yang Hanqing Hu Yihong Wu Xiongjie Lin Goucheng Fan Yongping Duan Charles Powell Veronica Ancona Muqing Zhang |
| author_facet | Chuanyu Yang Hanqing Hu Yihong Wu Xiongjie Lin Goucheng Fan Yongping Duan Charles Powell Veronica Ancona Muqing Zhang |
| author_sort | Chuanyu Yang |
| collection | DOAJ |
| description | Citrus huanglongbing (HLB) is a devastating disease for the citrus industry. The previous studies demonstrated that oxytetracycline and penicillin are effective antibiotics against <i>Candidatus</i> Liberibacter asiaticus (<i>C</i>Las). However, since <i>C</i>Las is uncultured, the mechanisms of action of antibiotics against <i>C</i>Las are still unclear. It was recently reported that the endophytic microbial communities are associated with the progression of citrus HLB after oxytetracycline and penicillin treatment. Therefore, we hypothesize that penicillin has greater antibacterial activity against <i>C</i>Las than oxytetracycline, which may be associated with the alteration of the structure and function of endophytic microbial communities in HLB-affected citrus in response to these antibiotics. To test this hypothesis, the microbiome of HLB-affected citrus leaves treated with these two antibiotics was analyzed using a metagenomic method. Our results indicate that the microbial structure and function in HLB-affected citrus were altered by these two antibiotics. The relative abundance of beneficial bacterial species, including <i>Streptomyces avermitilis</i> and <i>Bradyrhizobium,</i> was higher in penicillin-treated plants compared to those treated with oxytetracycline, and the relative abundance of the bacterial species (such as <i>Propionibacterium acnes</i> and <i>Synechocystis</i> sp PCC 6803) associated with <i>C</i>Las survival was lower for penicillin-treated plants compared to oxytetracycline-treated plants. These results indicate that penicillin has greater antibacterial activity against <i>C</i>Las. Based on the metagenomic analysis, this study elucidated the mechanism for the observed increase in antibacterial activity of penicillin against <i>C</i>Las. The data presented here are not only invaluable for developing eco-friendly and effective biocontrol strategies to combat citrus HLB, but also provide a method for revealing mechanism of antimicrobial against uncultured bacteria in host. |
| first_indexed | 2024-03-10T14:17:56Z |
| format | Article |
| id | doaj.art-e1faf48a851643279638e38bc49edc95 |
| institution | Directory Open Access Journal |
| issn | 2079-6382 |
| language | English |
| last_indexed | 2024-03-10T14:17:56Z |
| publishDate | 2020-12-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Antibiotics |
| spelling | doaj.art-e1faf48a851643279638e38bc49edc952023-11-20T23:38:08ZengMDPI AGAntibiotics2079-63822020-12-0191287410.3390/antibiotics9120874Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in PlantaChuanyu Yang0Hanqing Hu1Yihong Wu2Xiongjie Lin3Goucheng Fan4Yongping Duan5Charles Powell6Veronica Ancona7Muqing Zhang8Institute of Fruit Tree Research, Fujian Academy of Agricultural Sciences, Fuzhou 350003, ChinaInstitute of Fruit Tree Research, Fujian Academy of Agricultural Sciences, Fuzhou 350003, ChinaInstitute of Fruit Tree Research, Fujian Academy of Agricultural Sciences, Fuzhou 350003, ChinaInstitute of Fruit Tree Research, Fujian Academy of Agricultural Sciences, Fuzhou 350003, ChinaInstitute of Fruit Tree Research, Fujian Academy of Agricultural Sciences, Fuzhou 350003, ChinaUSHRL-USDA-ARS, 2011 S. Rock Rd, Fort Pierce, FL 34945, USAIRREC-IFAS, University of Florida, 2199 S. Rock Rd, Fort Pierce, FL 34945, USACitrus Center, Texas A&M University-Kingsville, 312 N. International Blvd, Weslaco, TX 785799, USAIRREC-IFAS, University of Florida, 2199 S. Rock Rd, Fort Pierce, FL 34945, USACitrus huanglongbing (HLB) is a devastating disease for the citrus industry. The previous studies demonstrated that oxytetracycline and penicillin are effective antibiotics against <i>Candidatus</i> Liberibacter asiaticus (<i>C</i>Las). However, since <i>C</i>Las is uncultured, the mechanisms of action of antibiotics against <i>C</i>Las are still unclear. It was recently reported that the endophytic microbial communities are associated with the progression of citrus HLB after oxytetracycline and penicillin treatment. Therefore, we hypothesize that penicillin has greater antibacterial activity against <i>C</i>Las than oxytetracycline, which may be associated with the alteration of the structure and function of endophytic microbial communities in HLB-affected citrus in response to these antibiotics. To test this hypothesis, the microbiome of HLB-affected citrus leaves treated with these two antibiotics was analyzed using a metagenomic method. Our results indicate that the microbial structure and function in HLB-affected citrus were altered by these two antibiotics. The relative abundance of beneficial bacterial species, including <i>Streptomyces avermitilis</i> and <i>Bradyrhizobium,</i> was higher in penicillin-treated plants compared to those treated with oxytetracycline, and the relative abundance of the bacterial species (such as <i>Propionibacterium acnes</i> and <i>Synechocystis</i> sp PCC 6803) associated with <i>C</i>Las survival was lower for penicillin-treated plants compared to oxytetracycline-treated plants. These results indicate that penicillin has greater antibacterial activity against <i>C</i>Las. Based on the metagenomic analysis, this study elucidated the mechanism for the observed increase in antibacterial activity of penicillin against <i>C</i>Las. The data presented here are not only invaluable for developing eco-friendly and effective biocontrol strategies to combat citrus HLB, but also provide a method for revealing mechanism of antimicrobial against uncultured bacteria in host.https://www.mdpi.com/2079-6382/9/12/874citrus Huanglongbingendophytic microbiomeoxytetracylinepenicillinmode of action |
| spellingShingle | Chuanyu Yang Hanqing Hu Yihong Wu Xiongjie Lin Goucheng Fan Yongping Duan Charles Powell Veronica Ancona Muqing Zhang Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta Antibiotics citrus Huanglongbing endophytic microbiome oxytetracyline penicillin mode of action |
| title | Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta |
| title_full | Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta |
| title_fullStr | Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta |
| title_full_unstemmed | Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta |
| title_short | Metagenomic Analysis Reveals the Mechanism for the Observed Increase in Antibacterial Activity of Penicillin against Uncultured Bacteria <i>Candidatus</i> Liberibacter asiaticus Relative to Oxytetracycline in Planta |
| title_sort | metagenomic analysis reveals the mechanism for the observed increase in antibacterial activity of penicillin against uncultured bacteria i candidatus i liberibacter asiaticus relative to oxytetracycline in planta |
| topic | citrus Huanglongbing endophytic microbiome oxytetracyline penicillin mode of action |
| url | https://www.mdpi.com/2079-6382/9/12/874 |
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