A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes
Abstract Background Examination of complex biological systems has long been achieved through methodical investigation of the system’s individual components. While informative, this strategy often leads to inappropriate conclusions about the system as a whole. With the advent of high-throughput “omic...
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| Format: | Article |
| Language: | English |
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BMC
2017-04-01
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| Series: | BMC Genomics |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12864-017-3708-4 |
| _version_ | 1811296036284530688 |
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| author | Sarah L. Grady Stephanie A. Malfatti Thusitha S. Gunasekera Brian K. Dalley Matt G. Lyman Richard C. Striebich Michael B. Mayhew Carol L. Zhou Oscar N. Ruiz Larry C. Dugan |
| author_facet | Sarah L. Grady Stephanie A. Malfatti Thusitha S. Gunasekera Brian K. Dalley Matt G. Lyman Richard C. Striebich Michael B. Mayhew Carol L. Zhou Oscar N. Ruiz Larry C. Dugan |
| author_sort | Sarah L. Grady |
| collection | DOAJ |
| description | Abstract Background Examination of complex biological systems has long been achieved through methodical investigation of the system’s individual components. While informative, this strategy often leads to inappropriate conclusions about the system as a whole. With the advent of high-throughput “omic” technologies, however, researchers can now simultaneously analyze an entire system at the level of molecule (DNA, RNA, protein, metabolite) and process (transcription, translation, enzyme catalysis). This strategy reduces the likelihood of improper conclusions, provides a framework for elucidation of genotype-phenotype relationships, and brings finer resolution to comparative genomic experiments. Here, we apply a multi-omic approach to analyze the gene expression profiles of two closely related Pseudomonas aeruginosa strains grown in n-alkanes or glycerol. Results The environmental P. aeruginosa isolate ATCC 33988 consumed medium-length (C10–C16) n-alkanes more rapidly than the laboratory strain PAO1, despite high genome sequence identity (average nucleotide identity >99%). Our data shows that ATCC 33988 induces a characteristic set of genes at the transcriptional, translational and post-translational levels during growth on alkanes, many of which differ from those expressed by PAO1. Of particular interest was the lack of expression from the rhl operon of the quorum sensing (QS) system, resulting in no measurable rhamnolipid production by ATCC 33988. Further examination showed that ATCC 33988 lacked the entire lasI/lasR arm of the QS response. Instead of promoting expression of QS genes, ATCC 33988 up-regulates a small subset of its genome, including operons responsible for specific alkaline proteases and sphingosine metabolism. Conclusion This work represents the first time results from RNA-seq, microarray, ribosome footprinting, proteomics, and small molecule LC-MS experiments have been integrated to compare gene expression in bacteria. Together, these data provide insights as to why strain ATCC 33988 is better adapted for growth and survival on n-alkanes. |
| first_indexed | 2024-04-13T05:42:29Z |
| format | Article |
| id | doaj.art-af4fef88fc8642e28521c5f190ece698 |
| institution | Directory Open Access Journal |
| issn | 1471-2164 |
| language | English |
| last_indexed | 2024-04-13T05:42:29Z |
| publishDate | 2017-04-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Genomics |
| spelling | doaj.art-af4fef88fc8642e28521c5f190ece6982022-12-22T03:00:03ZengBMCBMC Genomics1471-21642017-04-0118111910.1186/s12864-017-3708-4A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanesSarah L. Grady0Stephanie A. Malfatti1Thusitha S. Gunasekera2Brian K. Dalley3Matt G. Lyman4Richard C. Striebich5Michael B. Mayhew6Carol L. Zhou7Oscar N. Ruiz8Larry C. Dugan9Biosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National LaboratoryBiosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National LaboratoryEnvironmental Microbiology Group, University of Dayton Research Institute, University of DaytonHuntsman Cancer Institute, University of Utah School of MedicineBiosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National LaboratoryEnvironmental Microbiology Group, University of Dayton Research Institute, University of DaytonComputational Engineering Division, Lawrence Livermore National LaboratoryComputing Applications and Research Department, Global Security Computing and Applications Division, Lawrence Livermore National LaboratoryFuels and Energy Branch, Aerospace Systems Directorate, Air Force Research LaboratoryBiosciences and Biotechnology Division, Physical and Life Sciences Directorate, Lawrence Livermore National LaboratoryAbstract Background Examination of complex biological systems has long been achieved through methodical investigation of the system’s individual components. While informative, this strategy often leads to inappropriate conclusions about the system as a whole. With the advent of high-throughput “omic” technologies, however, researchers can now simultaneously analyze an entire system at the level of molecule (DNA, RNA, protein, metabolite) and process (transcription, translation, enzyme catalysis). This strategy reduces the likelihood of improper conclusions, provides a framework for elucidation of genotype-phenotype relationships, and brings finer resolution to comparative genomic experiments. Here, we apply a multi-omic approach to analyze the gene expression profiles of two closely related Pseudomonas aeruginosa strains grown in n-alkanes or glycerol. Results The environmental P. aeruginosa isolate ATCC 33988 consumed medium-length (C10–C16) n-alkanes more rapidly than the laboratory strain PAO1, despite high genome sequence identity (average nucleotide identity >99%). Our data shows that ATCC 33988 induces a characteristic set of genes at the transcriptional, translational and post-translational levels during growth on alkanes, many of which differ from those expressed by PAO1. Of particular interest was the lack of expression from the rhl operon of the quorum sensing (QS) system, resulting in no measurable rhamnolipid production by ATCC 33988. Further examination showed that ATCC 33988 lacked the entire lasI/lasR arm of the QS response. Instead of promoting expression of QS genes, ATCC 33988 up-regulates a small subset of its genome, including operons responsible for specific alkaline proteases and sphingosine metabolism. Conclusion This work represents the first time results from RNA-seq, microarray, ribosome footprinting, proteomics, and small molecule LC-MS experiments have been integrated to compare gene expression in bacteria. Together, these data provide insights as to why strain ATCC 33988 is better adapted for growth and survival on n-alkanes.http://link.springer.com/article/10.1186/s12864-017-3708-4Pseudomonas aeruginosaMulti-omicsRibosome footprintingQuorum sensingAlkane degradation |
| spellingShingle | Sarah L. Grady Stephanie A. Malfatti Thusitha S. Gunasekera Brian K. Dalley Matt G. Lyman Richard C. Striebich Michael B. Mayhew Carol L. Zhou Oscar N. Ruiz Larry C. Dugan A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes BMC Genomics Pseudomonas aeruginosa Multi-omics Ribosome footprinting Quorum sensing Alkane degradation |
| title | A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes |
| title_full | A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes |
| title_fullStr | A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes |
| title_full_unstemmed | A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes |
| title_short | A comprehensive multi-omics approach uncovers adaptations for growth and survival of Pseudomonas aeruginosa on n-alkanes |
| title_sort | comprehensive multi omics approach uncovers adaptations for growth and survival of pseudomonas aeruginosa on n alkanes |
| topic | Pseudomonas aeruginosa Multi-omics Ribosome footprinting Quorum sensing Alkane degradation |
| url | http://link.springer.com/article/10.1186/s12864-017-3708-4 |
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