The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm
Abstract Actinobacillus pleuropneumoniae is an important swine respiratory pathogen. Previous studies have suggested that growth as a biofilm is a natural state of A. pleuropneumoniae infection. To understand the survival features involved in the biofilm state, the growth features, morphology and ge...
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | Veterinary Research |
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| Online Access: | https://doi.org/10.1186/s13567-023-01173-x |
| _version_ | 1797817854530158592 |
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| author | Qiuhong Zhang Lu Peng Weiyao Han Hongyu Chen Hao Tang Xiabing Chen Paul R. Langford Qi Huang Rui Zhou Lu Li |
| author_facet | Qiuhong Zhang Lu Peng Weiyao Han Hongyu Chen Hao Tang Xiabing Chen Paul R. Langford Qi Huang Rui Zhou Lu Li |
| author_sort | Qiuhong Zhang |
| collection | DOAJ |
| description | Abstract Actinobacillus pleuropneumoniae is an important swine respiratory pathogen. Previous studies have suggested that growth as a biofilm is a natural state of A. pleuropneumoniae infection. To understand the survival features involved in the biofilm state, the growth features, morphology and gene expression profiles of planktonic and biofilm A. pleuropneumoniae were compared. A. pleuropneumoniae in biofilms showed reduced viability but maintained the presence of extracellular polymeric substances (EPS) after late log-phase. Under the microscope, bacteria in biofilms formed dense aggregated structures that were connected by abundant EPS, with reduced condensed chromatin. By construction of Δpga and ΔdspB mutants, polymeric β-1,6-linked N-acetylglucosamine and dispersin B were confirmed to be critical for normal biofilm formation. RNA-seq analysis indicated that, compared to their planktonic counterparts, A. pleuropneumoniae in biofilms had an extensively altered transcriptome. Carbohydrate metabolism, energy metabolism and translation were significantly repressed, while fermentation and genes contributing to EPS synthesis and translocation were up-regulated. The regulators Fnr (HlyX) and Fis were found to be up-regulated and their binding motifs were identified in the majority of the differentially expressed genes, suggesting their coordinated global role in regulating biofilm metabolism. By comparing the transcriptome of wild-type biofilm and Δpga, the utilization of oligosaccharides, iron and sulfur and fermentation were found to be important in adhesion and aggregation during biofilm formation. Additionally, when used as inocula, biofilm bacteria showed reduced virulence in mouse, compared with planktonic grown cells. Thus, these results have identified new facets of A. pleuropneumoniae biofilm maintenance and regulation. |
| first_indexed | 2024-03-13T08:59:35Z |
| format | Article |
| id | doaj.art-949784cb2c9540e3bf58a25244b2ef54 |
| institution | Directory Open Access Journal |
| issn | 1297-9716 |
| language | English |
| last_indexed | 2024-03-13T08:59:35Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | Veterinary Research |
| spelling | doaj.art-949784cb2c9540e3bf58a25244b2ef542023-05-28T11:25:03ZengBMCVeterinary Research1297-97162023-05-0154111810.1186/s13567-023-01173-xThe morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilmQiuhong Zhang0Lu Peng1Weiyao Han2Hongyu Chen3Hao Tang4Xiabing Chen5Paul R. Langford6Qi Huang7Rui Zhou8Lu Li9National Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityInstitute of Animal Husbandry and Veterinary Science, Wuhan Academy of Agricultural SciencesSection of Paediatric Infectious Disease, Imperial College LondonNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityNational Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural UniversityAbstract Actinobacillus pleuropneumoniae is an important swine respiratory pathogen. Previous studies have suggested that growth as a biofilm is a natural state of A. pleuropneumoniae infection. To understand the survival features involved in the biofilm state, the growth features, morphology and gene expression profiles of planktonic and biofilm A. pleuropneumoniae were compared. A. pleuropneumoniae in biofilms showed reduced viability but maintained the presence of extracellular polymeric substances (EPS) after late log-phase. Under the microscope, bacteria in biofilms formed dense aggregated structures that were connected by abundant EPS, with reduced condensed chromatin. By construction of Δpga and ΔdspB mutants, polymeric β-1,6-linked N-acetylglucosamine and dispersin B were confirmed to be critical for normal biofilm formation. RNA-seq analysis indicated that, compared to their planktonic counterparts, A. pleuropneumoniae in biofilms had an extensively altered transcriptome. Carbohydrate metabolism, energy metabolism and translation were significantly repressed, while fermentation and genes contributing to EPS synthesis and translocation were up-regulated. The regulators Fnr (HlyX) and Fis were found to be up-regulated and their binding motifs were identified in the majority of the differentially expressed genes, suggesting their coordinated global role in regulating biofilm metabolism. By comparing the transcriptome of wild-type biofilm and Δpga, the utilization of oligosaccharides, iron and sulfur and fermentation were found to be important in adhesion and aggregation during biofilm formation. Additionally, when used as inocula, biofilm bacteria showed reduced virulence in mouse, compared with planktonic grown cells. Thus, these results have identified new facets of A. pleuropneumoniae biofilm maintenance and regulation.https://doi.org/10.1186/s13567-023-01173-xActinobacillus pleuropneumoniaebiofilmplanktonicmorphologytranscriptionmetabolism |
| spellingShingle | Qiuhong Zhang Lu Peng Weiyao Han Hongyu Chen Hao Tang Xiabing Chen Paul R. Langford Qi Huang Rui Zhou Lu Li The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm Veterinary Research Actinobacillus pleuropneumoniae biofilm planktonic morphology transcription metabolism |
| title | The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm |
| title_full | The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm |
| title_fullStr | The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm |
| title_full_unstemmed | The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm |
| title_short | The morphology and metabolic changes of Actinobacillus pleuropneumoniae during its growth as a biofilm |
| title_sort | morphology and metabolic changes of actinobacillus pleuropneumoniae during its growth as a biofilm |
| topic | Actinobacillus pleuropneumoniae biofilm planktonic morphology transcription metabolism |
| url | https://doi.org/10.1186/s13567-023-01173-x |
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