Migratory Response of Soil Bacteria to
            <i>Lyophyllum</i>
            sp. Strain Karsten in Soil Microcosms

Warmink, Jan A.; Elsas, Jan Dirk van

doi:10.1128/aem.02110-08

Cited by 133 publications

(179 citation statements)

References 34 publications

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“…BS001 has been shown to migrate along growing fungal hyphae, a process potentially aided by the formation of a biofilm around the fungal tip (46,47). Similar to the induction of secondary bacterial carriage we see with the Burkholderia-D. discoideum interaction, BS001 appears to exert a "helper" effect, inducing the comigration of some nonmigratory bacterial species (48).…”

Section: Discussionmentioning

confidence: 65%

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Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

DiSalvo

Haselkorn

Bashir

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

104

239

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Symbiotic associations can allow an organism to acquire novel traits by accessing the genetic repertoire of its partner. In the Dictyostelium discoideum farming symbiosis, certain amoebas (termed “farmers”) stably associate with bacterial partners. Farmers can suffer a reproductive cost but also gain beneficial capabilities, such as carriage of bacterial food (proto-farming) and defense against competitors. Farming status previously has been attributed to amoeba genotype, but the role of bacterial partners in its induction has not been examined. Here, we explore the role of bacterial associates in the initiation, maintenance, and phenotypic effects of the farming symbiosis. We demonstrate that two clades of farmer-associated Burkholderia isolates colonize D. discoideum nonfarmers and infectiously endow them with farmer-like characteristics, indicating that Burkholderia symbionts are a major driver of the farming phenomenon. Under food-rich conditions, Burkholderia-colonized amoebas produce fewer spores than uncolonized counterparts, with the severity of this reduction being dependent on the Burkholderia colonizer. However, the induction of food carriage by Burkholderia colonization may be considered a conditionally adaptive trait because it can confer an advantage to the amoeba host when grown in food-limiting conditions. We observed Burkholderia inside and outside colonized D. discoideum spores after fruiting body formation; this observation, together with the ability of Burkholderia to colonize new amoebas, suggests a mixed mode of symbiont transmission. These results change our understanding of the D. discoideum farming symbiosis by establishing that the bacterial partner, Burkholderia, is an important causative agent of the farming phenomenon.

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Section: Discussionmentioning

confidence: 65%

“…One example of Burkholderia-eukaryote association that bears a particularly striking similarity to our system is the association of Burkholderia terrae strain BS001 with soil fungi (46). BS001 has been shown to migrate along growing fungal hyphae, a process potentially aided by the formation of a biofilm around the fungal tip (46,47).…”

Section: Discussionmentioning

confidence: 99%

Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

DiSalvo

Haselkorn

Bashir

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

104

239

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“…In contrast, B. fungorum, B. glathei, and B. sordidicola have been described as fungus-associated Burkholderia spp. (10,19,22,38). This shift toward fungusassociated species as roots progress from the juvenile to the senescent stage might be linked to the rapid decay of senescent roots, which constitute an ideal niche for organic matter-degrading fungi.…”

Section: Resultsmentioning

confidence: 99%

Burkholderia Species Are Major Inhabitants of White Lupin Cluster Roots

Weisskopf

Heller

Eberl

2011

Appl Environ Microbiol

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The formation of cluster roots by plants represents a highly efficient strategy for acquisition of sparingly available phosphate. This particular root type is characterized by a densely branched structure and high exudation of organic acids and protons, which are likely to influence the resident bacterial community. Until now, the identity of the bacterial populations living in cluster roots has not been investigated. We applied cultivation-dependent and cultivation-independent methods to characterize the dominant bacterial genera inhabiting the growing cluster roots of white lupin. We observed a high relative abundance of Burkholderia species (up to 58% of all isolated strains and 44% of all retrieved 16S rRNA sequences) and a significant enrichment with increasing cluster root age. Most of the sequences retrieved clustered together with known plant-or fungus-associated Burkholderia species, while only one of 98 sequences was affiliated with the Burkholderia cepacia complex. In vitro assays revealed that Burkholderia strains were much more tolerant to low pH than non-Burkholderia strains. Moreover, many strains produced large amounts of siderophores and were able to utilize citrate and oxalate as carbon sources. These features seem to represent important traits for the successful colonization and maintenance of Burkholderia species in white lupin cluster roots.To access sparingly available nutrients such as phosphate, plants have evolved several strategies, e.g., mycorrhizal association and cluster root formation. Cluster roots are very densely branched root structures with a particular excretion physiology (20,21,25). They occur in many species of the Proteaceae family and occasionally in the Mimosaceae, Casuarinaceae, or Fabaceae (7). White lupin is the only cluster-rooted species of agricultural importance and has thus been extensively studied (9,17,26,32,33,41,42). In white lupin, cluster root development follows a well-defined pattern: at the juvenile stage, cluster roots secrete small amounts of malate; at the mature stage, high quantities of citrate and protons are excreted, leading to drastic rhizosphere acidification; and at the senescent stage, organic acid excretion decreases. Besides citrate and malate, oxalate and fumarate have also been reported to be exuded by soil-grown lupin plants (6, 41). The close vicinity of growing cluster roots constitutes a highly selective environment, owing to rapid changes in pH and carbon availability. The abundance of bacteria, as well as richness and diversity, has been shown to decrease temporarily in mature cluster roots (40). However, the identity of the populations repressed or enriched during cluster root development has yet to be elucidated. We analyzed the bacterial communities living in the direct vicinity of cluster roots (root surface and inner tissues) by sequencing isolated strains and clone libraries constructed from root-extracted DNA. We then tested relevant physiological properties of isolates to better understand which metabolic abilities might ena...

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“…Biofilm formation on fungal surface may be beneficial in different ways like bacteria can exploit fungi as nutrient source directly or it can degrade complex substrates through production of extracellular enzymes. Bacterial cells colonizing fungal hyphae may use it to reach and colonize new microhabitats in soil [14,15]. Biofilm colonizing plant root surface provide better plant growth promotion as well as protection against several soil borne fungal pathogens [16].…”

Section: Introductionmentioning

confidence: 99%

Development of Mesorhizobium ciceri-Based Biofilms and Analyses of Their Antifungal and Plant Growth Promoting Activity in Chickpea Challenged by Fusarium Wilt

et al. 2016

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Biofilmed biofertilizers have emerged as a new improved inoculant technology to provide efficient nutrient and pest management and sustain soil fertility. In this investigation, development of a Trichoderma viride-Mesorhizobium ciceri biofilmed inoculant was undertaken, which we hypothesized, would possess more effective biological nitrogen fixing ability and plant growth promoting properties. As a novel attempt, we selected Mesorhizobium ciceri spp. with good antifungal attributes with the assumption that such inoculants could also serve as biocontrol agents. These biofilms exhibited significant enhancement in several plant growth promoting attributes, including 13-21 % increase in seed germination, production of ammonia, IAA and more than onefold to twofold enhancement in phosphate solubilisation, when compared to their individual partners. Enhancement of 10-11 % in antifungal activity against Fusarium oxysporum f. sp. ciceri was also recorded, over the respective M. ciceri counterparts. The effect of biofilms and the M. ciceri cultures individual on growth parameters of chickpea under pathogen challenged soil illustrated that the biofilms performed at par with the M. ciceri strains for most plant biometrical and disease related attributes. Elicitation of defense related enzymes like L-phenylalanine ammonia lyase, peroxidase and polyphenol oxidase was higher in M. ciceri/biofilm treated plants as compared to uninoculated plants under pathogen challenged soil. Further work on the signalling mechanisms among the partners and their tripartite interactions with host plant is envisaged in future studies.

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Migratory Response of Soil Bacteria to Lyophyllum sp. Strain Karsten in Soil Microcosms

Cited by 133 publications

References 34 publications

Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

Burkholderia bacteria infectiously induce the proto-farming symbiosis of Dictyostelium amoebae and food bacteria

Burkholderia Species Are Major Inhabitants of White Lupin Cluster Roots

Development of Mesorhizobium ciceri-Based Biofilms and Analyses of Their Antifungal and Plant Growth Promoting Activity in Chickpea Challenged by Fusarium Wilt

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