Genome variations between rhizosphere and bulk soil ecotypes of a Pseudomonas koreensis population

Bulk soil and rhizosphere are soil compartments selecting different microbial communities. However, it is unknown whether this selection also can change the genome content of specific bacterial taxa, splitting a population in distinct ecotypes. To answer this question we compared the genome sequences of 53 isolates obtained from sugarcane rhizosphere (28) and bulk soil (25). These isolates were previously classified in the Pseudomonas koreensis subgroup of the P. fluorescens complex. Phylogenomics showed a trend of separation between bulk soil and rhizosphere isolates. Discriminant analysis of principal components (DAPC) identified differences in the accessory genome of rhizosphere and bulk soil sub-populations. We found significant changes in gene frequencies distinguishing rhizosphere from bulk soil ecotypes, for example, enrichment of phosphatases and xylose utilization (xut) genes, respectively. Phenotypic assays and deletion of xutA gene indicated that accumulation of xut genes in the bulk soil sub-population provided a higher growth capacity in a d-xylose medium, supporting the corresponding genomic differences. Despite the clear differences distinguishing the two ecotypes, all 53 isolates were classified in a single 16S rRNA gene OTU. Collectively, our results revealed that the gene pool and ecological behavior of a bacterial population can be different for ecotypes living in neighbouring soil habitats.

[1]  Jeff H. Chang,et al.  Secondary Metabolism and Interspecific Competition Affect Accumulation of Spontaneous Mutants in the GacS-GacA Regulatory System in Pseudomonas protegens , 2018, mBio.

[2]  Omar E. Cornejo,et al.  Focusing the diversity of Gardnerella vaginalis through the lens of ecotypes , 2017, Evolutionary applications.

[3]  Edward W. Davis,et al.  Tropical soils are a reservoir for fluorescent Pseudomonas spp. biodiversity , 2018, Environmental microbiology.

[4]  J. L. Carvalho,et al.  Agronomic and environmental implications of sugarcane straw removal: a major review , 2017 .

[5]  V. Loux,et al.  Draft Genome Sequences of 18 Psychrotolerant and 2 Thermotolerant Strains Representative of Particular Ecotypes in the Bacillus cereus Group , 2017, Genome Announcements.

[6]  F. D. Andreote,et al.  Bacterial Abilities and Adaptation Toward the Rhizosphere Colonization , 2016, Front. Microbiol..

[7]  J. François,et al.  Engineering of a Synthetic Metabolic Pathway for the Assimilation of (d)-Xylose into Value-Added Chemicals. , 2016, ACS synthetic biology.

[8]  A new bacterial strain, Pseudomonas koreensis IB-4, as a promising agent for plant pathogen biological control , 2016, Microbiology.

[9]  Peer Bork,et al.  Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees , 2016, Nucleic Acids Res..

[10]  D. Karlen,et al.  Phosphorus pools responses to land-use change for sugarcane expansion in weathered Brazilian soils , 2016 .

[11]  Sagar M. Utturkar,et al.  Metabolic functions of Pseudomonas fluorescens strains from Populus deltoides depend on rhizosphere or endosphere isolation compartment , 2015, Front. Microbiol..

[12]  P. Rainey,et al.  Molecular mechanisms of xylose utilization by Pseudomonas fluorescens: overlapping genetic responses to xylose, xylulose, ribose and mannitol , 2015, Molecular microbiology.

[13]  T. Sokolova Specificity of soil properties in the rhizosphere: Analysis of literature data , 2015, Eurasian Soil Science.

[14]  Matthew R. Laird,et al.  IslandViewer 3: more flexible, interactive genomic island discovery, visualization and analysis , 2015, Nucleic Acids Res..

[15]  E. Blagodatskaya,et al.  Microbial hotspots and hot moments in soil: Concept & review , 2015 .

[16]  P. Shea,et al.  Potential use of Pseudomonas koreensis AGB-1 in association with Miscanthus sinensis to remediate heavy metal(loid)-contaminated mining site soil. , 2015, Journal of environmental management.

[17]  Robert G. Beiko,et al.  STAMP: statistical analysis of taxonomic and functional profiles , 2014, Bioinform..

[18]  E. Kuramae,et al.  Taxonomical and functional microbial community selection in soybean rhizosphere , 2014, The ISME Journal.

[19]  Torsten Seemann,et al.  Prokka: rapid prokaryotic genome annotation , 2014, Bioinform..

[20]  Otto X. Cordero,et al.  Explaining microbial genomic diversity in light of evolutionary ecology , 2014, Nature Reviews Microbiology.

[21]  Matthew Fraser,et al.  InterProScan 5: genome-scale protein function classification , 2014, Bioinform..

[22]  Alexandros Stamatakis,et al.  RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies , 2014, Bioinform..

[23]  G. Najafi,et al.  Lignocellulosic biomass to bioethanol, a comprehensive review with a focus on pretreatment , 2013 .

[24]  P. Lemanceau,et al.  Going back to the roots: the microbial ecology of the rhizosphere , 2013, Nature Reviews Microbiology.

[25]  B. Contreras-Moreira,et al.  GET_HOMOLOGUES, a Versatile Software Package for Scalable and Robust Microbial Pangenome Analysis , 2013, Applied and Environmental Microbiology.

[26]  Youn-Sig Kwak,et al.  Take-all of Wheat and Natural Disease Suppression: A Review , 2013, The plant pathology journal.

[27]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[28]  A. Klindworth,et al.  Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies , 2012, Nucleic acids research.

[29]  J. Ramos,et al.  Bacterial diversity in the rhizosphere of maize and the surrounding carbonate-rich bulk soil , 2012, Microbial biotechnology.

[30]  S. Sørensen,et al.  Assessment of the specificity of Burkholderia and Pseudomonas qPCR assays for detection of these genera in soil using 454 pyrosequencing. , 2012, FEMS microbiology letters.

[31]  Young Cheol Kim,et al.  Comparative Genomics of Plant-Associated Pseudomonas spp.: Insights into Diversity and Inheritance of Traits Involved in Multitrophic Interactions , 2012, PLoS genetics.

[32]  Sergey I. Nikolenko,et al.  SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing , 2012, J. Comput. Biol..

[33]  Otto X. Cordero,et al.  Population Genomics of Early Events in the Ecological Differentiation of Bacteria , 2012, Science.

[34]  M. Silby,et al.  Pseudomonas genomes: diverse and adaptable. , 2011, FEMS microbiology reviews.

[35]  David S. Wishart,et al.  PHAST: A Fast Phage Search Tool , 2011, Nucleic Acids Res..

[36]  P. Bakker,et al.  Deciphering the Rhizosphere Microbiome for Disease-Suppressive Bacteria , 2011, Science.

[37]  F. Balloux,et al.  Discriminant analysis of principal components: a new method for the analysis of genetically structured populations , 2010, BMC Genetics.

[38]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[39]  Paul G Dennis,et al.  Are root exudates more important than other sources of rhizodeposits in structuring rhizosphere bacterial communities? , 2010, FEMS microbiology ecology.

[40]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[41]  F. Martin,et al.  Pyrosequencing reveals a contrasted bacterial diversity between oak rhizosphere and surrounding soil. , 2010, Environmental microbiology reports.

[42]  B. Alsanius,et al.  Suppression of disease in tomato infected by Pythium ultimum with a biosurfactant produced by Pseudomonas koreensis , 2010, BioControl.

[43]  D. Falush Toward the Use of Genomics to Study Microevolutionary Change in Bacteria , 2009, PLoS genetics.

[44]  Gabriele Berg,et al.  Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. , 2009, FEMS microbiology ecology.

[45]  R. Friedman,et al.  Comparative genomics of two ecotypes of the marine planktonic copiotroph Alteromonas macleodii suggests alternative lifestyles associated with different kinds of particulate organic matter , 2008, The ISME Journal.

[46]  David R. Riley,et al.  Comparative genomics: the bacterial pan-genome. , 2008, Current opinion in microbiology.

[47]  Thibaut Jombart,et al.  adegenet: a R package for the multivariate analysis of genetic markers , 2008, Bioinform..

[48]  Lawrence A. David,et al.  Resource Partitioning and Sympatric Differentiation Among Closely Related Bacterioplankton , 2008, Science.

[49]  R. Costa,et al.  Pseudomonas community structure and antagonistic potential in the rhizosphere: insights gained by combining phylogenetic and functional gene-based analyses. , 2007, Environmental microbiology.

[50]  P. Bakker,et al.  Interactions between plants and beneficial Pseudomonas spp.: exploiting bacterial traits for crop protection , 2007, Antonie van Leeuwenhoek.

[51]  Laura E. Green,et al.  The role of ecological theory in microbial ecology , 2007, Nature Reviews Microbiology.

[52]  Georgios S. Vernikos,et al.  Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands , 2006, Bioinform..

[53]  Patricia Siguier,et al.  ISfinder: the reference centre for bacterial insertion sequences , 2005, Nucleic Acids Res..

[54]  Anil Lachke,et al.  Biofuel fromD-xylose — The second most abundant sugar , 2002 .

[55]  F. Cohan What are bacterial species? , 2002, Annual review of microbiology.

[56]  B. M. Gardener,et al.  Microbial populations responsible for specific soil suppressiveness to plant pathogens. , 2002, Annual review of phytopathology.

[57]  O Hammer-Muntz,et al.  PAST: paleontological statistics software package for education and data analysis version 2.09 , 2001 .

[58]  P. Lemanceau,et al.  Effect of Two Plant Species, Flax (Linum usitatissinum L.) and Tomato (Lycopersicon esculentum Mill.), on the Diversity of Soilborne Populations of Fluorescent Pseudomonads , 1995, Applied and environmental microbiology.

[59]  Ronald M. Atlas,et al.  Handbook of microbiological media , 1993 .

[60]  S. Levy,et al.  Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. , 1988, Applied and environmental microbiology.