Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species
Abstract Background Rhizosphere microorganisms play a crucial role in plant health and development. Plant root exudates (PRE) are a complex mixture of organic molecules and provide nutritional and signaling information to rhizosphere microorganisms. Burkholderiaceae species are non-abundant in the r...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-09-01
|
| Series: | BMC Microbiology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12866-022-02633-8 |
| _version_ | 1811267696392667136 |
|---|---|
| author | Javier Ignacio Cillero Pablo Andrés Henríquez Thomas Warwick Ledger Gonzalo Andrés Ruz Bernardo González |
| author_facet | Javier Ignacio Cillero Pablo Andrés Henríquez Thomas Warwick Ledger Gonzalo Andrés Ruz Bernardo González |
| author_sort | Javier Ignacio Cillero |
| collection | DOAJ |
| description | Abstract Background Rhizosphere microorganisms play a crucial role in plant health and development. Plant root exudates (PRE) are a complex mixture of organic molecules and provide nutritional and signaling information to rhizosphere microorganisms. Burkholderiaceae species are non-abundant in the rhizosphere but exhibit a wide range of plant-growth-promoting and plant-health-protection effects. Most of these plant-associated microorganisms have been studied in isolation under laboratory conditions, whereas in nature, they interact in competition or cooperation with each other. To improve our understanding of the factors driving growth dynamics of low-abundant bacterial species in the rhizosphere, we hypothesized that the growth and survival of four Burkholderiaceae strains (Paraburkholderia phytofirmans PsJN, Cupriavidus metallidurans CH34, C. pinatubonensis JMP134 and C. taiwanensis LMG19424) in Arabidopsis thaliana PRE is affected by the presence of each other. Results Differential growth abilities of each strain were found depending on plant age and whether PRE was obtained after growth on N limitation conditions. The best-adapted strain to grow in PRE was P. phytofirmans PsJN, with C. pinatubonensis JMP134 growing better than the other two Cupriavidus strains. Individual strain behavior changed when they succeeded in combinations. Clustering analysis showed that the 4-member co-culture grouped with one of the best-adapted strains, either P. phytofirmans PsJN or C. pinatubonensis JMP134, depending on the PRE used. Sequential transference experiments showed that the behavior of the 4-member co-culture relies on the type of PRE provided for growth. Conclusions The results suggest that individual strain behavior changed when they grew in combinations of two, three, or four members, and those changes are determined first by the inherent characteristics of each strain and secondly by the environment. |
| first_indexed | 2024-04-12T21:07:18Z |
| format | Article |
| id | doaj.art-78ae938e4bb5488286820e53c572df18 |
| institution | Directory Open Access Journal |
| issn | 1471-2180 |
| language | English |
| last_indexed | 2024-04-12T21:07:18Z |
| publishDate | 2022-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Microbiology |
| spelling | doaj.art-78ae938e4bb5488286820e53c572df182022-12-22T03:16:40ZengBMCBMC Microbiology1471-21802022-09-0122111410.1186/s12866-022-02633-8Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae speciesJavier Ignacio Cillero0Pablo Andrés Henríquez1Thomas Warwick Ledger2Gonzalo Andrés Ruz3Bernardo González4Laboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo IbáñezFacultad de Economía y Empresa, Universidad Diego PortalesLaboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo IbáñezLaboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo IbáñezLaboratorio de Bioingeniería, Facultad de Ingeniería y Ciencias, Universidad Adolfo IbáñezAbstract Background Rhizosphere microorganisms play a crucial role in plant health and development. Plant root exudates (PRE) are a complex mixture of organic molecules and provide nutritional and signaling information to rhizosphere microorganisms. Burkholderiaceae species are non-abundant in the rhizosphere but exhibit a wide range of plant-growth-promoting and plant-health-protection effects. Most of these plant-associated microorganisms have been studied in isolation under laboratory conditions, whereas in nature, they interact in competition or cooperation with each other. To improve our understanding of the factors driving growth dynamics of low-abundant bacterial species in the rhizosphere, we hypothesized that the growth and survival of four Burkholderiaceae strains (Paraburkholderia phytofirmans PsJN, Cupriavidus metallidurans CH34, C. pinatubonensis JMP134 and C. taiwanensis LMG19424) in Arabidopsis thaliana PRE is affected by the presence of each other. Results Differential growth abilities of each strain were found depending on plant age and whether PRE was obtained after growth on N limitation conditions. The best-adapted strain to grow in PRE was P. phytofirmans PsJN, with C. pinatubonensis JMP134 growing better than the other two Cupriavidus strains. Individual strain behavior changed when they succeeded in combinations. Clustering analysis showed that the 4-member co-culture grouped with one of the best-adapted strains, either P. phytofirmans PsJN or C. pinatubonensis JMP134, depending on the PRE used. Sequential transference experiments showed that the behavior of the 4-member co-culture relies on the type of PRE provided for growth. Conclusions The results suggest that individual strain behavior changed when they grew in combinations of two, three, or four members, and those changes are determined first by the inherent characteristics of each strain and secondly by the environment.https://doi.org/10.1186/s12866-022-02633-8ArabidopsisBacterial growthBurkholderiaceaeCo-cultureRoot exudates |
| spellingShingle | Javier Ignacio Cillero Pablo Andrés Henríquez Thomas Warwick Ledger Gonzalo Andrés Ruz Bernardo González Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species BMC Microbiology Arabidopsis Bacterial growth Burkholderiaceae Co-culture Root exudates |
| title | Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species |
| title_full | Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species |
| title_fullStr | Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species |
| title_full_unstemmed | Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species |
| title_short | Individual competence predominates over host nutritional status in Arabidopsis root exudate-mediated bacterial enrichment in a combination of four Burkholderiaceae species |
| title_sort | individual competence predominates over host nutritional status in arabidopsis root exudate mediated bacterial enrichment in a combination of four burkholderiaceae species |
| topic | Arabidopsis Bacterial growth Burkholderiaceae Co-culture Root exudates |
| url | https://doi.org/10.1186/s12866-022-02633-8 |
| work_keys_str_mv | AT javierignaciocillero individualcompetencepredominatesoverhostnutritionalstatusinarabidopsisrootexudatemediatedbacterialenrichmentinacombinationoffourburkholderiaceaespecies AT pabloandreshenriquez individualcompetencepredominatesoverhostnutritionalstatusinarabidopsisrootexudatemediatedbacterialenrichmentinacombinationoffourburkholderiaceaespecies AT thomaswarwickledger individualcompetencepredominatesoverhostnutritionalstatusinarabidopsisrootexudatemediatedbacterialenrichmentinacombinationoffourburkholderiaceaespecies AT gonzaloandresruz individualcompetencepredominatesoverhostnutritionalstatusinarabidopsisrootexudatemediatedbacterialenrichmentinacombinationoffourburkholderiaceaespecies AT bernardogonzalez individualcompetencepredominatesoverhostnutritionalstatusinarabidopsisrootexudatemediatedbacterialenrichmentinacombinationoffourburkholderiaceaespecies |