Nudzejma Stulanovic, Yasmine Kerdel, Lucas Rezende, Benoit Deflandre, Pierre Burguet, Loïc Belde, Romane Denoel, Déborah Tellatin, Augustin Rigolet, Marc Hanikenne, Loïc Quinton, Marc Ongena, Sébastien Rigali
{"title":"氮源增强了嗜苷酸介导的马铃薯普通疮痂病和晚疫病病原菌之间对铁的竞争。","authors":"Nudzejma Stulanovic, Yasmine Kerdel, Lucas Rezende, Benoit Deflandre, Pierre Burguet, Loïc Belde, Romane Denoel, Déborah Tellatin, Augustin Rigolet, Marc Hanikenne, Loïc Quinton, Marc Ongena, Sébastien Rigali","doi":"10.1093/mtomcs/mfae004","DOIUrl":null,"url":null,"abstract":"<p><p>How do pathogens affecting the same host interact with each other? We evaluated here the types of microbe-microbe interactions taking place between Streptomyces scabiei and Phytophthora infestans, the causative agents of common scab and late blight diseases in potato crops, respectively. Under most laboratory culture conditions tested, S. scabiei impaired or completely inhibited the growth of P. infestans by producing either soluble and/or volatile compounds. Increasing peptone levels correlated with increased inhibition of P. infestans. Comparative metabolomics showed that production of S. scabiei siderophores (desferrioxamines, pyochelin, scabichelin, and turgichelin) increased with the quantity of peptone, thereby suggesting that they participate in the inhibition of the oomycete growth. Mass spectrometry imaging further uncovered that the zones of secreted siderophores and of P. infestans growth inhibition coincided. Moreover, either the repression of siderophore production or the neutralization of their iron-chelating activity led to a resumption of P. infestans growth. Replacement of peptone by natural nitrogen sources such as ammonium nitrate, sodium nitrate, ammonium sulfate, and urea also triggered siderophore production in S. scabiei. Interestingly, nitrogen source-induced siderophore production also inhibited the growth of Alternaria solani, the causative agent of the potato early blight. Overall, our work further emphasizes the importance of competition for iron between microorganisms that colonize the same niche. As common scab never alters the vegetative propagation of tubers, we propose that S. scabiei, under certain conditions, could play a protective role for its hosts against much more destructive pathogens through exploitative iron competition and volatile compound production.</p>","PeriodicalId":89,"journal":{"name":"Metallomics","volume":" ","pages":""},"PeriodicalIF":2.9000,"publicationDate":"2024-02-07","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Nitrogen sources enhance siderophore-mediated competition for iron between potato common scab and late blight causative agents.\",\"authors\":\"Nudzejma Stulanovic, Yasmine Kerdel, Lucas Rezende, Benoit Deflandre, Pierre Burguet, Loïc Belde, Romane Denoel, Déborah Tellatin, Augustin Rigolet, Marc Hanikenne, Loïc Quinton, Marc Ongena, Sébastien Rigali\",\"doi\":\"10.1093/mtomcs/mfae004\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>How do pathogens affecting the same host interact with each other? We evaluated here the types of microbe-microbe interactions taking place between Streptomyces scabiei and Phytophthora infestans, the causative agents of common scab and late blight diseases in potato crops, respectively. Under most laboratory culture conditions tested, S. scabiei impaired or completely inhibited the growth of P. infestans by producing either soluble and/or volatile compounds. Increasing peptone levels correlated with increased inhibition of P. infestans. Comparative metabolomics showed that production of S. scabiei siderophores (desferrioxamines, pyochelin, scabichelin, and turgichelin) increased with the quantity of peptone, thereby suggesting that they participate in the inhibition of the oomycete growth. Mass spectrometry imaging further uncovered that the zones of secreted siderophores and of P. infestans growth inhibition coincided. Moreover, either the repression of siderophore production or the neutralization of their iron-chelating activity led to a resumption of P. infestans growth. Replacement of peptone by natural nitrogen sources such as ammonium nitrate, sodium nitrate, ammonium sulfate, and urea also triggered siderophore production in S. scabiei. Interestingly, nitrogen source-induced siderophore production also inhibited the growth of Alternaria solani, the causative agent of the potato early blight. Overall, our work further emphasizes the importance of competition for iron between microorganisms that colonize the same niche. As common scab never alters the vegetative propagation of tubers, we propose that S. scabiei, under certain conditions, could play a protective role for its hosts against much more destructive pathogens through exploitative iron competition and volatile compound production.</p>\",\"PeriodicalId\":89,\"journal\":{\"name\":\"Metallomics\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":2.9000,\"publicationDate\":\"2024-02-07\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Metallomics\",\"FirstCategoryId\":\"99\",\"ListUrlMain\":\"https://doi.org/10.1093/mtomcs/mfae004\",\"RegionNum\":3,\"RegionCategory\":\"生物学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q3\",\"JCRName\":\"BIOCHEMISTRY & MOLECULAR BIOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Metallomics","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1093/mtomcs/mfae004","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q3","JCRName":"BIOCHEMISTRY & MOLECULAR BIOLOGY","Score":null,"Total":0}
引用次数: 0
摘要
影响同一宿主的病原体如何相互作用?我们在此评估了马铃薯作物常见疮痂病和晚疫病的病原菌--疮痂链霉菌(Streptomyces scabiei)和疫霉菌(Phytophthora infestans)之间的微生物相互作用类型。在大多数测试的实验室培养条件下,疮痂霉通过产生可溶性和/或挥发性化合物来抑制或完全抑制侵染病菌的生长。蛋白胨含量的增加与对 P. infestans 的抑制作用增强相关。代谢组学比较显示,疮痂病菌嗜苷酸盐(去铁氧胺、pyochelin、scabichelin 和 turgichelin)的产生量随蛋白胨含量的增加而增加,这表明它们参与了对卵菌生长的抑制作用。质谱成像进一步发现,分泌苷元的区域和 P. infestans 的生长抑制区域是一致的。此外,抑制嗜苷酸盐的产生或中和其螯合铁的活性都会导致 P. infestans 恢复生长。用天然氮源(如硝酸铵、硝酸钠、硫酸铵和尿素)替代蛋白胨也会引发疥螨产生嗜铁素。有趣的是,氮源诱导的嗜苷酸的产生也抑制了马铃薯早疫病的病原菌 Alternaria solani 的生长。总之,我们的工作进一步强调了定殖于同一生态位的微生物之间对铁的竞争的重要性。由于普通疮痂病从未改变块茎的无性繁殖,我们建议疮痂病菌在某些条件下可以通过利用铁竞争和产生挥发性化合物来保护宿主免受更具破坏性的病原体的侵害。
Nitrogen sources enhance siderophore-mediated competition for iron between potato common scab and late blight causative agents.
How do pathogens affecting the same host interact with each other? We evaluated here the types of microbe-microbe interactions taking place between Streptomyces scabiei and Phytophthora infestans, the causative agents of common scab and late blight diseases in potato crops, respectively. Under most laboratory culture conditions tested, S. scabiei impaired or completely inhibited the growth of P. infestans by producing either soluble and/or volatile compounds. Increasing peptone levels correlated with increased inhibition of P. infestans. Comparative metabolomics showed that production of S. scabiei siderophores (desferrioxamines, pyochelin, scabichelin, and turgichelin) increased with the quantity of peptone, thereby suggesting that they participate in the inhibition of the oomycete growth. Mass spectrometry imaging further uncovered that the zones of secreted siderophores and of P. infestans growth inhibition coincided. Moreover, either the repression of siderophore production or the neutralization of their iron-chelating activity led to a resumption of P. infestans growth. Replacement of peptone by natural nitrogen sources such as ammonium nitrate, sodium nitrate, ammonium sulfate, and urea also triggered siderophore production in S. scabiei. Interestingly, nitrogen source-induced siderophore production also inhibited the growth of Alternaria solani, the causative agent of the potato early blight. Overall, our work further emphasizes the importance of competition for iron between microorganisms that colonize the same niche. As common scab never alters the vegetative propagation of tubers, we propose that S. scabiei, under certain conditions, could play a protective role for its hosts against much more destructive pathogens through exploitative iron competition and volatile compound production.