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Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response.

Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M - Front Microbiol (2016)

Bottom Line: Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI.Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death.These differences are discussed in the frame of a multilayered response to non self in fungi.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et Génétique Cellulaire, UMR 5095, Centre National de la Recherche Scientifique et Université de Bordeaux Bordeaux, France.

ABSTRACT
Recognition and response to non self is essential to development and survival of all organisms. It can occur between individuals of the same species or between different organisms. Fungi are established models for conspecific non self recognition in the form of vegetative incompatibility (VI), a genetically controlled process initiating a programmed cell death (PCD) leading to the rejection of a fusion cell between genetically different isolates of the same species. In Podospora anserina VI is controlled by members of the hnwd gene family encoding for proteins analogous to NOD Like Receptors (NLR) immune receptors in eukaryotes. It was hypothesized that the hnwd controlled VI reaction was derived from the fungal innate immune response. Here we analyze the P. anserina transcriptional responses to two bacterial species, Serratia fonticola to which P. anserina survives and S. marcescens to which P. anserina succumbs, and compare these to the transcriptional response induced under VI conditions. Transcriptional responses to both bacteria largely overlap, however the number of genes regulated and magnitude of regulation is more important when P. anserina survives. Transcriptional responses to bacteria also overlap with the VI reaction for both up or down regulated gene sets. Genes up regulated tend to be clustered in the genome, and display limited phylogenetic distribution. In all three responses we observed genes related to autophagy to be up-regulated. Autophagy contributes to the fungal survival in all three conditions. Genes encoding for secondary metabolites and histidine kinase signaling are also up regulated in all three conditions. Transcriptional responses also display differences. Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI. Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death. These differences are discussed in the frame of a multilayered response to non self in fungi.

No MeSH data available.


Related in: MedlinePlus

Autophagy exerts a pro-survival function in response to bacteria. (A,B) Light or atg1 autophagy mutant ∆ Evans blue staining of WT (A) or (B) 6 h after transfer onto a S. fonticola seeded plate. (C,D) Cell death level measure atg8 autophagy mutants after transfer onto S. ∆pspA, and ∆atg1, ∆ for WT, fonticola (C) or S. marcescens(D) seeded plates. Cell death was estimated from 10 different pictures of three independent experiments for each time point (two tailed t-test, *p < 0.05, **p < 0.001).
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Figure 7: Autophagy exerts a pro-survival function in response to bacteria. (A,B) Light or atg1 autophagy mutant ∆ Evans blue staining of WT (A) or (B) 6 h after transfer onto a S. fonticola seeded plate. (C,D) Cell death level measure atg8 autophagy mutants after transfer onto S. ∆pspA, and ∆atg1, ∆ for WT, fonticola (C) or S. marcescens(D) seeded plates. Cell death was estimated from 10 different pictures of three independent experiments for each time point (two tailed t-test, *p < 0.05, **p < 0.001).

Mentions: Autophagy, the only GO term associated with all three responses, is generally associated to stress responses (Kroemer et al., 2010), and has also been described as essential to immune response in plants and animals (Zhou et al., 2014; Benoit et al., 2015; Shibutani et al., 2015). Genes encoding components of the S. cerevisiae autophagy machinery were recently reviewed (Feng et al., 2014). Eighteen have orthologs in P. anserina, 12, 10, and 12 of which are up regulated in the VsSf, VsSm, or VI gene sets while none is down regulated (Additional file 4). The role of autophagy as a cell death or survival mechanism seems to depend on the context and model (Dickman and Fluhr, 2013). Autophagy has been extensively studied in P. anserina, in particular in the context of VI where it exerts a pro-survival function, and was hypothesized to restrict spread of death signals from the heterokaryotic cell (Pinan-Lucarré et al., 2005, 2007). We transferred three P. anserina autophagy mutants, ΔPa-ATG1, ΔPa-ATG8 (Pinan-Lucarré et al., 2005), and ΔpspA (Paoletti et al., 2001) involved at different stages of the process onto S. fonticola or S. marcescens seeded plates. In presence of both bacteria, autophagy mutant cell death rapidly reaches high levels not attained by WT strain (60–80%) (Figure 7). This is particularly clear in transfer to S. fonticola seeded plates, while in response to S. marcescens level of WT cell death is initially slightly inferior to that of the autophagy mutant strains. These results indicate that as for VI, autophagy exerts a pro-survival function in response to bacteria. This pro-survival function of autophagy is the clearest in response to S. fonticola, but seems attenuated in response to S. marcescens. Interestingly S. marcescens is known to be able to alter the pH of autophagic like vesicles in mammalian cells (Fedrigo et al., 2011) and one could speculate that such action renders autophagy less efficient in P. anserina as well.


Overlapping Podospora anserina Transcriptional Responses to Bacterial and Fungal Non Self Indicate a Multilayered Innate Immune Response.

Lamacchia M, Dyrka W, Breton A, Saupe SJ, Paoletti M - Front Microbiol (2016)

Autophagy exerts a pro-survival function in response to bacteria. (A,B) Light or atg1 autophagy mutant ∆ Evans blue staining of WT (A) or (B) 6 h after transfer onto a S. fonticola seeded plate. (C,D) Cell death level measure atg8 autophagy mutants after transfer onto S. ∆pspA, and ∆atg1, ∆ for WT, fonticola (C) or S. marcescens(D) seeded plates. Cell death was estimated from 10 different pictures of three independent experiments for each time point (two tailed t-test, *p < 0.05, **p < 0.001).
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Related In: Results  -  Collection

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Figure 7: Autophagy exerts a pro-survival function in response to bacteria. (A,B) Light or atg1 autophagy mutant ∆ Evans blue staining of WT (A) or (B) 6 h after transfer onto a S. fonticola seeded plate. (C,D) Cell death level measure atg8 autophagy mutants after transfer onto S. ∆pspA, and ∆atg1, ∆ for WT, fonticola (C) or S. marcescens(D) seeded plates. Cell death was estimated from 10 different pictures of three independent experiments for each time point (two tailed t-test, *p < 0.05, **p < 0.001).
Mentions: Autophagy, the only GO term associated with all three responses, is generally associated to stress responses (Kroemer et al., 2010), and has also been described as essential to immune response in plants and animals (Zhou et al., 2014; Benoit et al., 2015; Shibutani et al., 2015). Genes encoding components of the S. cerevisiae autophagy machinery were recently reviewed (Feng et al., 2014). Eighteen have orthologs in P. anserina, 12, 10, and 12 of which are up regulated in the VsSf, VsSm, or VI gene sets while none is down regulated (Additional file 4). The role of autophagy as a cell death or survival mechanism seems to depend on the context and model (Dickman and Fluhr, 2013). Autophagy has been extensively studied in P. anserina, in particular in the context of VI where it exerts a pro-survival function, and was hypothesized to restrict spread of death signals from the heterokaryotic cell (Pinan-Lucarré et al., 2005, 2007). We transferred three P. anserina autophagy mutants, ΔPa-ATG1, ΔPa-ATG8 (Pinan-Lucarré et al., 2005), and ΔpspA (Paoletti et al., 2001) involved at different stages of the process onto S. fonticola or S. marcescens seeded plates. In presence of both bacteria, autophagy mutant cell death rapidly reaches high levels not attained by WT strain (60–80%) (Figure 7). This is particularly clear in transfer to S. fonticola seeded plates, while in response to S. marcescens level of WT cell death is initially slightly inferior to that of the autophagy mutant strains. These results indicate that as for VI, autophagy exerts a pro-survival function in response to bacteria. This pro-survival function of autophagy is the clearest in response to S. fonticola, but seems attenuated in response to S. marcescens. Interestingly S. marcescens is known to be able to alter the pH of autophagic like vesicles in mammalian cells (Fedrigo et al., 2011) and one could speculate that such action renders autophagy less efficient in P. anserina as well.

Bottom Line: Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI.Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death.These differences are discussed in the frame of a multilayered response to non self in fungi.

View Article: PubMed Central - PubMed

Affiliation: Institut de Biologie et Génétique Cellulaire, UMR 5095, Centre National de la Recherche Scientifique et Université de Bordeaux Bordeaux, France.

ABSTRACT
Recognition and response to non self is essential to development and survival of all organisms. It can occur between individuals of the same species or between different organisms. Fungi are established models for conspecific non self recognition in the form of vegetative incompatibility (VI), a genetically controlled process initiating a programmed cell death (PCD) leading to the rejection of a fusion cell between genetically different isolates of the same species. In Podospora anserina VI is controlled by members of the hnwd gene family encoding for proteins analogous to NOD Like Receptors (NLR) immune receptors in eukaryotes. It was hypothesized that the hnwd controlled VI reaction was derived from the fungal innate immune response. Here we analyze the P. anserina transcriptional responses to two bacterial species, Serratia fonticola to which P. anserina survives and S. marcescens to which P. anserina succumbs, and compare these to the transcriptional response induced under VI conditions. Transcriptional responses to both bacteria largely overlap, however the number of genes regulated and magnitude of regulation is more important when P. anserina survives. Transcriptional responses to bacteria also overlap with the VI reaction for both up or down regulated gene sets. Genes up regulated tend to be clustered in the genome, and display limited phylogenetic distribution. In all three responses we observed genes related to autophagy to be up-regulated. Autophagy contributes to the fungal survival in all three conditions. Genes encoding for secondary metabolites and histidine kinase signaling are also up regulated in all three conditions. Transcriptional responses also display differences. Genes involved in response to oxidative stress, or encoding small secreted proteins are essentially expressed in response to bacteria, while genes encoding NLR proteins are expressed during VI. Most functions encoded in response to bacteria favor survival of the fungus while most functions up regulated during VI would lead to cell death. These differences are discussed in the frame of a multilayered response to non self in fungi.

No MeSH data available.


Related in: MedlinePlus