In Situ Identification of Intracellular Bacteria Related to
            <i>Paenibacillus</i>
            spp. in the Mycelium of the Ectomycorrhizal Fungus
            <i>Laccaria bicolor</i>
            S238N

Bertaux, Joanne; Schmid, Michael; Prevost-Boure, N. Chemidlin; Churin, Jean-Louis; Hartmann, Anton; Garbaye, Jean; Frey‐Klett, Pascale

doi:10.1128/aem.69.7.4243-4248.2003

Cited by 128 publications

(94 citation statements)

References 34 publications

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“…Fluorescence in situ hybridization using a Rhizobium-specific probe confirmed the stable endocellular association of small numbers of RrF4 cells within P. indica chlamydospores and hyphae, and a ratio of 0.035 ng of bacterial DNA per 100 ng of P. indica DNA was determined by quantitative PCR (qPCR) analysis (Sharma et al, 2008). This result coincides well with the low number of different bacteria (1-20 per fungal cell) that were detected in the ectomycorrhiza fungus Laccaria bicolor (Bertaux et al, 2003;Bertaux et al, 2005). Intriguingly, RrF4 could be isolated from powdered fungal mycelia and propagated in axenic cultures, showing that the bacterium is not entirely dependent on its fungal host.…”

Section: Introductionsupporting

confidence: 61%

“…Endofungal bacteria were previously detected in Glomeromycotan arbuscular mycorrhiza symbioses (Bonfante and Anca, 2009;Naumann et al, 2010), in the ectomycorrhizal fungus Laccaria bicolor (Bertaux et al, 2003(Bertaux et al, , 2005, in the rice pathogenic fungus Rhizopus microsporus (Partida-Martinez and Hertweck, 2005), in hyphae of phylogenetically diverse foliar fungal endophytes (Hoffman and Arnold, 2010), in the soil isolate Mortierella alpina (Kai et al, 2012) and the plant symbiotic Endogone Mucoromycotina fungi (Desirò et al, 2015). Endofungal bacteria, associated with fungi of the genera Piriformospora and Sebacina, belong to two genera of Gram-negative (Rhizobium and Acinetobacter) and two genera of Gram-positive (Paenibacillus and Rhodococcus) bacteria.…”

Section: Introductionmentioning

confidence: 99%

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Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

et al. 2015

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The Alphaproteobacterium Rhizobium radiobacter F4 (RrF4) was originally characterized as an endofungal bacterium in the beneficial endophytic Sebacinalean fungus Piriformospora indica. Although attempts to cure P. indica from RrF4 repeatedly failed, the bacterium can easily be grown in pure culture. Here, we report on RrF4's genome and the beneficial impact the free-living bacterium has on plants. In contrast to other endofungal bacteria, the genome size of RrF4 is not reduced. Instead, it shows a high degree of similarity to the plant pathogenic R. radiobacter (formerly: Agrobacterium tumefaciens) C58, except vibrant differences in both the tumor-inducing (pTi) and the accessor (pAt) plasmids, which can explain the loss of RrF4's pathogenicity. Similar to its fungal host, RrF4 colonizes plant roots without host preference and forms aggregates of attached cells and dense biofilms at the root surface of maturation zones. RrF4-colonized plants show increased biomass and enhanced resistance against bacterial leaf pathogens. Mutational analysis showed that, similar to P. indica, resistance mediated by RrF4 was dependent on the plant's jasmonate-based induced systemic resistance (ISR) pathway. Consistent with this, RrF4-and P. indica-induced pattern of defense gene expression were similar. In clear contrast to P. indica, but similar to plant growth-promoting rhizobacteria, RrF4 colonized not only the root outer cortex but also spread beyond the endodermis into the stele. On the basis of our findings, RrF4 is an efficient plant growth-promoting bacterium.

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Section: Introductionsupporting

confidence: 61%

Section: Introductionmentioning

confidence: 99%

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

et al. 2015

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“…Partial sequencing of the 16S ribosomal DNA genes of the bacterial isolates was carried out as described by Bertaux et al (7). After purification, the 16S ribosomal DNA gene products were sequenced with the eubacterial primer 27F (60).…”

Section: Bacterial Strains (I) Originmentioning

confidence: 99%

Root-Associated Bacteria Contribute to Mineral Weathering and to Mineral Nutrition in Trees: a Budgeting Analysis

Calvaruso

Turpault²,

Frey‐Klett

2006

Appl Environ Microbiol

196

101

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The principal nutrient source for forest trees derives from the weathering of soil minerals which results from water circulation and from plant and microbial activity. The main objectives of this work were to quantify the respective effects of plant-and root-associated bacteria on mineral weathering and their consequences on tree seedling growth and nutrition. That is why we carried out two column experiments with a quartz-biotite substrate. The columns were planted with or without pine seedlings and inoculated or not with three ectomycorrhizosphere bacterial strains to quantify biotite weathering and pine growth and to determine how bacteria improve pine growth. We showed that the pine roots significantly increased biotite weathering by a factor of 1.3 for magnesium and 1.7 for potassium. We also demonstrated that the inoculation of Burkholderia glathei PML1(12) significantly increased biotite weathering by a factor of 1.4 for magnesium and 1.5 for potassium in comparison with the pine alone. In addition, we observed a significant positive effect of B. glathei PMB1(7) and PML1(12) on pine growth and on root morphology (number of lateral roots and root hairs). We demonstrated that PML1(12) improved pine growth when the seedlings were supplied with a nutrient solution which did not contain the nutrients present in the biotite. No improvement of pine growth was observed when the seedlings were supplied with all the nutrients necessary for pine growth. We therefore propose that the growth-promoting effect of B. glathei PML1(12) mainly resulted from the improved plant nutrition via increased mineral weathering.In ecosystems with low inputs and without any fertilization or soil amendment by humans, the nutrients available to plants come from atmospheric inputs and weathering of soil minerals. This is mainly the case with forest ecosystems which, in addition, are frequently located on poor and acidic soils (3). Plants developing on acidic soils are subjected to two major constraints: (i) high concentrations of ions like Al 3ϩ and H ϩ which inhibit root growth and (ii) low mineral nutrient availability as a result of low reserves and impaired uptake due to high H ϩ concentrations (40).In temperate and boreal forest ecosystems, the vast majority of trees live in close association with symbiotic fungi, the ectomycorrhizal fungi, which connect tree roots to the soil environment via a broad network of hyphae. These fungi contribute to plant nutrition by carrying far away from the roots and from very small pores, the water and the nutrients they released by weathering the primary minerals (30, 59). In addition, the ectomycorrhizal symbiosis modifies root exudation qualitatively and quantitatively by changing the metabolic functions of the roots (34, 51, 56). It creates a special environment called mycorrhizosphere, where the bacterial equilibrium is different from that of the bulk soil (soil without any influence of roots) (36). These modifications of the bacterial equilibrium in the mycorrhizosphere are likely to contribut...

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“…These examples, coupled with the discovery of bacteria within hyphae of the ectomycorrhizal Dikarya (Tuber borchii; Ascomycota; Laccaria bicolor and Piriformospora indica; Basidiomycota) (5)(6)(7)(8)58), suggest that the capacity to harbor endohyphal bacteria is widespread among fungi. To date, however, endocellular bacteria have been recovered only from fungi that occur in the soil and rhizosphere (12,31).…”

mentioning

confidence: 99%

Diverse Bacteria Inhabit Living Hyphae of Phylogenetically Diverse Fungal Endophytes

Hoffman

Arnold

2010

Appl Environ Microbiol

229

224

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Both the establishment and outcomes of plant-fungus symbioses can be influenced by abiotic factors, the interplay of fungal and plant genotypes, and additional microbes associated with fungal mycelia. Recently bacterial endosymbionts were documented in soilborne Glomeromycota and Mucoromycotina and in at least one species each of mycorrhizal Basidiomycota and Ascomycota. Here we show for the first time that phylogenetically diverse endohyphal bacteria occur in living hyphae of diverse foliar endophytes, including representatives of four classes of Ascomycota. We examined 414 isolates of endophytic fungi, isolated from photosynthetic tissues of six species of cupressaceous trees in five biogeographic provinces, for endohyphal bacteria using microscopy and molecular techniques. Viable bacteria were observed within living hyphae of endophytic Pezizomycetes, Dothideomycetes, Eurotiomycetes, and Sordariomycetes from all tree species and biotic regions surveyed. A focus on 29 fungus/bacterium associations revealed that bacterial and fungal phylogenies were incongruent with each other and with taxonomic relationships of host plants. Overall, eight families and 15 distinct genotypes of endohyphal bacteria were recovered; most were members of the Proteobacteria, but a small number of Bacillaceae also were found, including one that appears to occur as an endophyte of plants. Frequent loss of bacteria following subculturing suggests a facultative association. Our study recovered distinct lineages of endohyphal bacteria relative to previous studies, is the first to document their occurrence in foliar endophytes representing four of the most species-rich classes of fungi, and highlights for the first time their diversity and phylogenetic relationships with regard both to the endophytes they inhabit and the plants in which these endophyte-bacterium symbiota occur.Traits related to the establishment and outcome of plantfungus symbioses can reflect not only abiotic conditions and the unique interactions of particular fungal and plant genotypes (49,50,56,59,62,67) but also additional microbes that interact intimately with fungal mycelia (4, 12, 42). For example, mycorrhizosphere-associated actinomycetes release volatile compounds that influence spore germination in the arbuscular mycorrhizal (AM) fungus Gigaspora margarita (Glomeromycota) (14). Levy et al. (34) describe Burkholderia spp. that colonize spores and hyphae of the AM fungus Gigaspora decipiens and are associated with decreased spore germination. Diverse "helper" bacteria have been implicated in promoting hyphal growth and the establishment of ectomycorrhizal symbioses (23,26,57,70). Minerdi et al. (43) found that a consortium of ectosymbiotic bacteria limited the ability of the pathogen Fusarium oxysporum to infect and cause vascular wilts in lettuce, with virulence restored to the pathogen when ectosymbionts were removed.In addition to interacting with environmental and ectosymbiotic bacteria, some plant-associated fungi harbor bacteria within their hyphae (first ...

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In Situ Identification of Intracellular Bacteria Related to Paenibacillus spp. in the Mycelium of the Ectomycorrhizal Fungus Laccaria bicolor S238N

Cited by 128 publications

References 34 publications

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

Non-pathogenic Rhizobium radiobacter F4 deploys plant beneficial activity independent of its host Piriformospora indica

Root-Associated Bacteria Contribute to Mineral Weathering and to Mineral Nutrition in Trees: a Budgeting Analysis

Diverse Bacteria Inhabit Living Hyphae of Phylogenetically Diverse Fungal Endophytes

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