A Coevolutionary Framework for Managing Disease-Suppressive Soils

Kinkel, Linda L.; Bakker, Matthew G.; Schlatter, Daniel

doi:10.1146/annurev-phyto-072910-095232

Cited by 199 publications

(174 citation statements)

References 130 publications

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“…Deeper understanding of the diverse roles of antibiotics in species interactions in soil, the dynamics of antibiotic inhibition in natural habitats and especially the factors that may determine the potential for a coevolutionary arms race vs coevolutionary differentiation are crucial for understanding the long-term trajectories of antibiotic-producing microbes in soil. Recent work suggests the potential for soil edaphic characteristics, nutrient availability or nutrient diversity in soil, physical environmental stress and phylogeny to predict microbial inhibitory activities and coevolutionary interactions in soil populations (Schlatter et al, 2009;Bakker et al, 2010;Kinkel et al, 2011;Bailey and Kassen, 2012;Otto-Hanson et al, 2013). More detailed understanding of the precise roles of these factors in mediating microbial species interactions and coevolution in soil will contribute significantly to the search for novel antibiotic biochemistries, to enhanced insight into the maintenance of antibiotic resistance genes in environmental microbes and to management of disease suppressive activity of indigenous soil microbes (Martinez et al, 2011;Kinkel et al, 2011;Kinkel et al, 2012 …”

Section: Resistance Interactions Among Sympatric and Allopatric Isolamentioning

confidence: 99%

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

et al. 2013

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Soil bacteria produce a diverse array of antibiotics, yet our understanding of the specific roles of antibiotics in the ecological and evolutionary dynamics of microbial interactions in natural habitats remains limited. Here, we show a significant role for antibiotics in mediating antagonistic interactions and nutrient competition among locally coexisting Streptomycete populations from soil. We found that antibiotic inhibition is significantly more intense among sympatric than allopatric Streptomycete populations, indicating local selection for inhibitory phenotypes. For sympatric but not allopatric populations, antibiotic inhibition is significantly positively correlated with niche overlap, indicating that inhibition is targeted toward bacteria that pose the greatest competitive threat. Our results support the hypothesis that antibiotics serve as weapons in mediating local microbial interactions in soil and suggest that coevolutionary niche displacement may reduce the likelihood of an antibiotic arms race. Further insight into the diverse roles of antibiotics in microbial ecology and evolution has significant implications for understanding the persistence of antibiotic inhibitory and resistance phenotypes in environmental microbes, optimizing antibiotic drug discovery and developing strategies for managing microbial coevolutionary dynamics to enhance inhibitory phenotypes.

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Section: Resistance Interactions Among Sympatric and Allopatric Isolamentioning

confidence: 99%

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

et al. 2013

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“…The concepts of medical intervention in prevention of infectious disease have lately been expanded to include not only vaccination for host immunological preparation, but also organic reconstitution of healthy human microbiota using fecal transplants (Brandt & Aroniadis, 2013;Damman et al, 2012;Lemon et al, 2012). In well-documented environmental studies, the diversity and population ecology of antagonistic Streptomyces in soil have been shown to co-evolve which has implications for plant disease suppression (Kinkel et al, 2011(Kinkel et al, , 2012. Has nature thus provided us with possible novel therapeutic strategies for CF?…”

Section: Prospects For Treatmentmentioning

confidence: 99%

Chronic pulmonary pseudomonal infection in patients with cystic fibrosis: A model for early phase symbiotic evolution

Qin

2014

Critical Reviews in Microbiology

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To cite this article: Xuan Qin (2016) Chronic pulmonary pseudomonal infection in patients with cystic fibrosis: A model for early phase symbiotic evolution, Critical Reviews in Microbiology, 42:1, 144-157, DOI: 10.3109/1040841X.2014 AbstractGain of ''antimicrobial resistance'' and ''adaptive virulence'' has been the dominant view of Pseudomonas aeruginosa (Pa) in cystic fibrosis (CF) in the progressively damaged host airway over the course of this chronic infection. However, the pathogenic effects of CF airway-adapted Pa strains are notably reduced. We propose that CF Pa and other bacterial cohabitants undergo host adaptation which resembles the changes found in bacterial symbionts in animal hosts. Development of clonally selected and intraspecific isogenic Pa strains which display divergent colony morphology, growth rate, auxotrophy, and antibiotic susceptibility in vitro suggests an adaptive sequence of infective exploitation-parasitism-symbiotic evolution driven by host defenses. Most importantly, the emergence of CF pseudomonal auxotrophy is frequently associated with a few specific amino acids. The selective retention or loss of specific amino acid biosynthesis in CF-adapted Pa reflects bacterium-host symbiosis and coevolution during chronic infection, not nutrient availability. This principle also argues against the long-standing concept of dietary availability leading to evolution of essential amino acid requirements in humans. A novel model of pseudomonal adaptation through multicellular bacterial syntrophy is proposed to explain early events in bacterial gene decay and decreased (not increased) virulence due to symbiotic response to host defense.

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“…However, interaction between plants and microbes is more general with plants shown to shape the rhizosphere microbiota in legumes, potatoes and suppressive soils (Sharma et al, 2005;Lebreton et al, 2007;Manter et al, 2010;Kinkel et al, 2011;Mendes et al, 2011;Turner et al, 2013b). Some microbial root colonists are saprophytes, which also colonise splinters of wood inserted into soil (Bulgarelli et al, 2012), but others are selected by exudation of nutrient sources and phytoalexins, such as glucosinolates and avenacins (Sonderby et al, 2007;Bressan et al, 2009;Turner et al, 2013b).…”

Section: Introductionmentioning

confidence: 99%

“…Some microbial root colonists are saprophytes, which also colonise splinters of wood inserted into soil (Bulgarelli et al, 2012), but others are selected by exudation of nutrient sources and phytoalexins, such as glucosinolates and avenacins (Sonderby et al, 2007;Bressan et al, 2009;Turner et al, 2013b). Furthermore, by altering the rhizosphere microbiota, plants induce formation of suppressive soil where growth of plant pathogens is inhibited (Lebreton et al, 2007;Kinkel et al, 2011;Mendes et al, 2011). Microbes can increase plant growth by releasing phytohormones, biofertilization (Lugtenberg and Kamilova, 2009) and stimulation of both the induced systemic resistance and systemic-acquired resistance components of the plant immune system (Van der Ent et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition

et al. 2015

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We examined succession of the rhizosphere microbiota of three model plants (Arabidopsis, Medicago and Brachypodium) in compost and sand and three crops (Brassica, Pisum and Triticum) in compost alone. We used serial inoculation of 24 independent replicate microcosms over three plant generations for each plant/soil combination. Stochastic variation between replicates was surprisingly weak and by the third generation, replicate microcosms for each plant had communities that were very similar to each other but different to those of other plants or unplanted soil. Microbiota diversity remained high in compost, but declined drastically in sand, with bacterial opportunists and putative autotrophs becoming dominant. These dramatic differences indicate that many microbes cannot thrive on plant exudates alone and presumably also require carbon sources and/or nutrients from soil. Arabidopsis had the weakest influence on its microbiota and in compost replicate microcosms converged on three alternative community compositions rather than a single distinctive community. Organisms selected in rhizospheres can have positive or negative effects. Two abundant bacteria are shown to promote plant growth, but in Brassica the pathogen Olpidium brassicae came to dominate the fungal community. So plants exert strong selection on the rhizosphere microbiota but soil composition is critical to its stability. microbial succession/ plant-microbe interactions/rhizosphere microbiota/selection.

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A Coevolutionary Framework for Managing Disease-Suppressive Soils

Cited by 199 publications

References 130 publications

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

Sympatric inhibition and niche differentiation suggest alternative coevolutionary trajectories among Streptomycetes

Chronic pulmonary pseudomonal infection in patients with cystic fibrosis: A model for early phase symbiotic evolution

Stability and succession of the rhizosphere microbiota depends upon plant type and soil composition

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