Background: The maternal gut microbiome is the direct and important source of early colonization and development of the neonatal gut microbiome. However, differences in unique and shared features between mothers with different physiological phenotypes and their newborns still lack exhaustive investigation. Here, using a cow-to-calf model, a comprehensive investigation was conducted to elucidate the pattern and characterization of microbial transfer from the maternal source to the offspring.
Results: The microbiota in the rumen and feces of dairy cows were divided into two clusters via enterotype analysis. The cows from the enterotype distinguished by Prevotella in the rumen had better production performance, whereas no difference was observed in the cows classified by feces enterotype. Furthermore, through a pairwise combination of fecal and ruminal enterotypes, we screened a group of dairy cows with excellent phenotypes. The gastrointestinal microbiomes of cows with different phenotypes and their offspring differed significantly. The rumen was a more important microbial source for meconium than feces. Transmission of beneficial bacteria from mother to offspring was observed. Additionally, the meconium inherits advantageous metabolic functions of the rumen. The resistome features of the rumen, feces, and meconium were consistent, and resistome abundance from cows to calves showed an expanding trend. The interaction between antibiotic-resistance genes and mobile genetic elements from the rumen to meconium was the most remarkable. The diversity of core metabolites from cows to calves was stable and not affected by differences in phenotypes. However, the abundance of specific metabolites varied greatly.
Conclusions: Our study demonstrates the microbial taxa, metabolic function, and resistome characteristics of maternal and neonatal microbiomes, and reveals the potential vertical transmission of the microbiome from a cow-to-calf model. These findings provide new insights into the transgenerational transmission pattern of the microbiome. Video Abstract.
{"title":"Maternal gastrointestinal microbiome shapes gut microbial function and resistome of newborns in a cow-to-calf model.","authors":"Yimin Zhuang, Shuai Liu, Duo Gao, Yiming Xu, Wen Jiang, Guobin Hou, Sumin Li, Xinjie Zhao, Tianyu Chen, Shangru Li, Siyuan Zhang, Yanting Huang, Jingjun Wang, Jianxin Xiao, Mengmeng Li, Wei Wang, Shengli Li, Zhijun Cao","doi":"10.1186/s40168-024-01943-5","DOIUrl":"https://doi.org/10.1186/s40168-024-01943-5","url":null,"abstract":"<p><strong>Background: </strong>The maternal gut microbiome is the direct and important source of early colonization and development of the neonatal gut microbiome. However, differences in unique and shared features between mothers with different physiological phenotypes and their newborns still lack exhaustive investigation. Here, using a cow-to-calf model, a comprehensive investigation was conducted to elucidate the pattern and characterization of microbial transfer from the maternal source to the offspring.</p><p><strong>Results: </strong>The microbiota in the rumen and feces of dairy cows were divided into two clusters via enterotype analysis. The cows from the enterotype distinguished by Prevotella in the rumen had better production performance, whereas no difference was observed in the cows classified by feces enterotype. Furthermore, through a pairwise combination of fecal and ruminal enterotypes, we screened a group of dairy cows with excellent phenotypes. The gastrointestinal microbiomes of cows with different phenotypes and their offspring differed significantly. The rumen was a more important microbial source for meconium than feces. Transmission of beneficial bacteria from mother to offspring was observed. Additionally, the meconium inherits advantageous metabolic functions of the rumen. The resistome features of the rumen, feces, and meconium were consistent, and resistome abundance from cows to calves showed an expanding trend. The interaction between antibiotic-resistance genes and mobile genetic elements from the rumen to meconium was the most remarkable. The diversity of core metabolites from cows to calves was stable and not affected by differences in phenotypes. However, the abundance of specific metabolites varied greatly.</p><p><strong>Conclusions: </strong>Our study demonstrates the microbial taxa, metabolic function, and resistome characteristics of maternal and neonatal microbiomes, and reveals the potential vertical transmission of the microbiome from a cow-to-calf model. These findings provide new insights into the transgenerational transmission pattern of the microbiome. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"216"},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495063/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503481","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-22DOI: 10.1186/s40168-024-01913-x
Ralf Rosenstein, Benjamin O Torres Salazar, Claudia Sauer, Simon Heilbronner, Bernhard Krismer, Andreas Peschel
Background: Bacterial pathogens such as Staphylococcus aureus colonize body surfaces of part of the human population, which represents a critical risk factor for skin disorders and invasive infections. However, such pathogens do not belong to the human core microbiomes. Beneficial commensal bacteria can often prevent the invasion and persistence of such pathogens by using molecular strategies that are only superficially understood. We recently reported that the commensal bacterium Staphylococcus lugdunensis produces the novel antibiotic lugdunin, which eradicates S. aureus from the nasal microbiomes of hospitalized patients. However, it has remained unclear if S. lugdunensis may affect S. aureus carriage in the general population and which external factors might promote S. lugdunensis carriage to enhance its S. aureus-eliminating capacity.
Results: We could cultivate S. lugdunensis from the noses of 6.3% of healthy human volunteers. In addition, S. lugdunensis DNA could be identified in metagenomes of many culture-negative nasal samples indicating that cultivation success depends on a specific bacterial threshold density. Healthy S. lugdunensis carriers had a 5.2-fold lower propensity to be colonized by S. aureus indicating that lugdunin can eliminate S. aureus also in healthy humans. S. lugdunensis-positive microbiomes were dominated by either Staphylococcus epidermidis, Corynebacterium species, or Dolosigranulum pigrum. These and further bacterial commensals, whose abundance was positively associated with S. lugdunensis, promoted S. lugdunensis growth in co-culture. Such mutualistic interactions depended on the production of iron-scavenging siderophores by supportive commensals and on the capacity of S. lugdunensis to import siderophores. Video Abstract CONCLUSIONS: These findings underscore the importance of microbiome homeostasis for eliminating pathogen colonization. Elucidating mechanisms that drive microbiome interactions will become crucial for microbiome-precision editing approaches.
背景:金黄色葡萄球菌等细菌病原体定植于部分人群的体表,是导致皮肤病和侵入性感染的重要风险因素。然而,这类病原体并不属于人类核心微生物组。有益的共生细菌通常可以利用分子策略阻止这类病原体的入侵和持续存在,但人们对这些策略的了解还很肤浅。我们最近报告说,共生细菌卢格杜恩葡萄球菌能产生新型抗生素卢格杜宁,它能根除住院患者鼻腔微生物组中的金黄色葡萄球菌。然而,目前仍不清楚卢格杜菌是否会影响普通人群中的金黄色葡萄球菌携带,以及哪些外部因素可能会促进卢格杜菌的携带,从而增强其消灭金黄色葡萄球菌的能力:结果:我们可以从 6.3% 的健康志愿者鼻腔中培养出卢格登氏菌。此外,在许多培养阴性的鼻腔样本的元基因组中可以鉴定出 S. lugdunensis DNA,这表明培养成功与否取决于特定的细菌阈值密度。健康的 S. lugdunensis 携带者被金黄色葡萄球菌定植的可能性降低了 5.2 倍,这表明 lugdunin 也能消灭健康人体内的金黄色葡萄球菌。卢格杜氏菌阳性微生物组主要由表皮葡萄球菌、棒状杆菌或猪多糖所组成。这些细菌和其他细菌共生体(其丰度与 S. lugdunensis 呈正相关)在共培养中促进了 S. lugdunensis 的生长。这种互利的相互作用取决于支持性共生菌产生的铁清除嗜苷酸盐以及卢格氏菌输入嗜苷酸盐的能力。视频摘要 结论:这些发现强调了微生物组平衡对消除病原体定植的重要性。阐明驱动微生物组相互作用的机制将成为微生物组精确编辑方法的关键。
{"title":"The Staphylococcus aureus-antagonizing human nasal commensal Staphylococcus lugdunensis depends on siderophore piracy.","authors":"Ralf Rosenstein, Benjamin O Torres Salazar, Claudia Sauer, Simon Heilbronner, Bernhard Krismer, Andreas Peschel","doi":"10.1186/s40168-024-01913-x","DOIUrl":"https://doi.org/10.1186/s40168-024-01913-x","url":null,"abstract":"<p><strong>Background: </strong>Bacterial pathogens such as Staphylococcus aureus colonize body surfaces of part of the human population, which represents a critical risk factor for skin disorders and invasive infections. However, such pathogens do not belong to the human core microbiomes. Beneficial commensal bacteria can often prevent the invasion and persistence of such pathogens by using molecular strategies that are only superficially understood. We recently reported that the commensal bacterium Staphylococcus lugdunensis produces the novel antibiotic lugdunin, which eradicates S. aureus from the nasal microbiomes of hospitalized patients. However, it has remained unclear if S. lugdunensis may affect S. aureus carriage in the general population and which external factors might promote S. lugdunensis carriage to enhance its S. aureus-eliminating capacity.</p><p><strong>Results: </strong>We could cultivate S. lugdunensis from the noses of 6.3% of healthy human volunteers. In addition, S. lugdunensis DNA could be identified in metagenomes of many culture-negative nasal samples indicating that cultivation success depends on a specific bacterial threshold density. Healthy S. lugdunensis carriers had a 5.2-fold lower propensity to be colonized by S. aureus indicating that lugdunin can eliminate S. aureus also in healthy humans. S. lugdunensis-positive microbiomes were dominated by either Staphylococcus epidermidis, Corynebacterium species, or Dolosigranulum pigrum. These and further bacterial commensals, whose abundance was positively associated with S. lugdunensis, promoted S. lugdunensis growth in co-culture. Such mutualistic interactions depended on the production of iron-scavenging siderophores by supportive commensals and on the capacity of S. lugdunensis to import siderophores. Video Abstract CONCLUSIONS: These findings underscore the importance of microbiome homeostasis for eliminating pathogen colonization. Elucidating mechanisms that drive microbiome interactions will become crucial for microbiome-precision editing approaches.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"213"},"PeriodicalIF":13.8,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11495082/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142503494","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-21DOI: 10.1186/s40168-024-01914-w
Xingang Zhou, Jingyu Zhang, Jibo Shi, Muhammad Khashi U Rahman, Hongwei Liu, Zhong Wei, Fengzhi Wu, Francisco Dini-Andreote
Background: Volatile organic compounds (VOCs) released by plants can act as signaling molecules mediating ecological interactions. Therefore, the study of VOCs mediated intra- and interspecific interactions with downstream plant physiological responses is critical to advance our understanding of mechanisms underlying information exchange in plants. Here, we investigated how plant-emitted VOCs affect the performance of an interspecific neighboring plant via induced shifts in root exudate chemistry with implications for root-associated microbiota recruitment.
Results: First, we showed that VOCs emitted by potato-onion plants stimulate the growth of adjacent tomato plants. Then, we demonstrated that this positive effect on tomato biomass was attributed to shifts in the tomato rhizosphere microbiota. Specifically, we found potato-onion VOCs to indirectly affect the recruitment of specific bacteria (e.g., Pseudomonas and Bacillus spp.) in the tomato rhizosphere. Second, we identified and validated the compound dipropyl disulfide as the active molecule within the blend of potato-onion VOCs mediating this interspecific plant communication. Third, we showed that the effect on the tomato rhizosphere microbiota occurs via induced changes in root exudates of tomato plants caused by exposure to dipropyl disulfide. Last, Pseudomonas and Bacillus spp. bacteria enriched in the tomato rhizosphere were shown to have plant growth-promoting activities.
Conclusions: Potato-onion VOCs-specifically dipropyl disulfide-can induce shifts in the root exudate of adjacent tomato plants, which results in the recruitment of plant-beneficial bacteria in the rhizosphere. Taken together, this study elucidated a new mechanism of interspecific plant interaction mediated by VOCs resulting in alterations in the rhizosphere microbiota with beneficial outcomes for plant performance. Video Abstract.
{"title":"Volatile-mediated interspecific plant interaction promotes root colonization by beneficial bacteria via induced shifts in root exudation.","authors":"Xingang Zhou, Jingyu Zhang, Jibo Shi, Muhammad Khashi U Rahman, Hongwei Liu, Zhong Wei, Fengzhi Wu, Francisco Dini-Andreote","doi":"10.1186/s40168-024-01914-w","DOIUrl":"10.1186/s40168-024-01914-w","url":null,"abstract":"<p><strong>Background: </strong>Volatile organic compounds (VOCs) released by plants can act as signaling molecules mediating ecological interactions. Therefore, the study of VOCs mediated intra- and interspecific interactions with downstream plant physiological responses is critical to advance our understanding of mechanisms underlying information exchange in plants. Here, we investigated how plant-emitted VOCs affect the performance of an interspecific neighboring plant via induced shifts in root exudate chemistry with implications for root-associated microbiota recruitment.</p><p><strong>Results: </strong>First, we showed that VOCs emitted by potato-onion plants stimulate the growth of adjacent tomato plants. Then, we demonstrated that this positive effect on tomato biomass was attributed to shifts in the tomato rhizosphere microbiota. Specifically, we found potato-onion VOCs to indirectly affect the recruitment of specific bacteria (e.g., Pseudomonas and Bacillus spp.) in the tomato rhizosphere. Second, we identified and validated the compound dipropyl disulfide as the active molecule within the blend of potato-onion VOCs mediating this interspecific plant communication. Third, we showed that the effect on the tomato rhizosphere microbiota occurs via induced changes in root exudates of tomato plants caused by exposure to dipropyl disulfide. Last, Pseudomonas and Bacillus spp. bacteria enriched in the tomato rhizosphere were shown to have plant growth-promoting activities.</p><p><strong>Conclusions: </strong>Potato-onion VOCs-specifically dipropyl disulfide-can induce shifts in the root exudate of adjacent tomato plants, which results in the recruitment of plant-beneficial bacteria in the rhizosphere. Taken together, this study elucidated a new mechanism of interspecific plant interaction mediated by VOCs resulting in alterations in the rhizosphere microbiota with beneficial outcomes for plant performance. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"207"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492557/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469621","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Background: The disease resistance phenotype is closely related to immunomodulatory function and immune tolerance and has far-reaching implications in animal husbandry and human health. Microbes play an important role in the initiation, prevention, and treatment of diseases, but the mechanisms of host-microbiota interactions in disease-resistant phenotypes are poorly understood. In this study, we hope to uncover and explain the role of microbes in intestinal diseases and their mechanisms of action to identify new potential treatments.
Methods: First, we established the colitis model of DSS in two breeds of sheep and then collected the samples for multi-omics testing including metagenes, metabolome, and transcriptome. Next, we made the fecal bacteria liquid from the four groups of sheep feces collected from H-CON, H-DSS, E-CON, and E-DSS to transplant the fecal bacteria into mice. H-CON feces were transplanted into mice named HH group and H-DSS feces were transplanted into mice named HD group and Roseburia bacteria treatment named HDR groups. E-CON feces were transplanted into mice named EH group and E-DSS feces were transplanted into mice in the ED group and Roseburia bacteria treatment named EDR groups. After successful modeling, samples were taken for multi-omics testing. Finally, colitis mice in HD group and ED group were administrated with Roseburia bacteria, and the treatment effect was evaluated by H&E, PAS, immunohistochemistry, and other experimental methods.
Results: The difference in disease resistance of sheep to DSS-induced colitis disease is mainly due to the increase in the abundance of Roseburia bacteria and the increase of bile acid secretion in the intestinal tract of Hu sheep in addition to the accumulation of potentially harmful bacteria in the intestine when the disease occurs, which makes the disease resistance of Hu sheep stronger under the same disease conditions. However, the enrichment of harmful microorganisms in East Friesian sheep activated the TNFα signalling pathway, which aggravated the intestinal injury, and then the treatment of FMT mice by culturing Roseburia bacteria found that Roseburia bacteria had a good curative effect on colitis.
Conclusion: Our study showed that in H-DSS-treated sheep, the intestinal barrier is stabilized with an increase in the abundance of beneficial microorganisms. Our data also suggest that Roseburia bacteria have a protective effect on the intestinal barrier of Hu sheep. Accumulating evidence suggests that host-microbiota interactions are associated with IBD disease progression. Video Abstract.
{"title":"Host-microbe interaction-mediated resistance to DSS-induced inflammatory enteritis in sheep.","authors":"Shuo Yan, Ruilin Du, Wenna Yao, Huimin Zhang, Yue Xue, Teligun, Yongfa Li, Hanggai Bao, Yulong Zhao, Shuo Cao, Guifang Cao, Xihe Li, Siqin Bao, Yongli Song","doi":"10.1186/s40168-024-01932-8","DOIUrl":"10.1186/s40168-024-01932-8","url":null,"abstract":"<p><strong>Background: </strong>The disease resistance phenotype is closely related to immunomodulatory function and immune tolerance and has far-reaching implications in animal husbandry and human health. Microbes play an important role in the initiation, prevention, and treatment of diseases, but the mechanisms of host-microbiota interactions in disease-resistant phenotypes are poorly understood. In this study, we hope to uncover and explain the role of microbes in intestinal diseases and their mechanisms of action to identify new potential treatments.</p><p><strong>Methods: </strong>First, we established the colitis model of DSS in two breeds of sheep and then collected the samples for multi-omics testing including metagenes, metabolome, and transcriptome. Next, we made the fecal bacteria liquid from the four groups of sheep feces collected from H-CON, H-DSS, E-CON, and E-DSS to transplant the fecal bacteria into mice. H-CON feces were transplanted into mice named HH group and H-DSS feces were transplanted into mice named HD group and Roseburia bacteria treatment named HDR groups. E-CON feces were transplanted into mice named EH group and E-DSS feces were transplanted into mice in the ED group and Roseburia bacteria treatment named EDR groups. After successful modeling, samples were taken for multi-omics testing. Finally, colitis mice in HD group and ED group were administrated with Roseburia bacteria, and the treatment effect was evaluated by H&E, PAS, immunohistochemistry, and other experimental methods.</p><p><strong>Results: </strong>The difference in disease resistance of sheep to DSS-induced colitis disease is mainly due to the increase in the abundance of Roseburia bacteria and the increase of bile acid secretion in the intestinal tract of Hu sheep in addition to the accumulation of potentially harmful bacteria in the intestine when the disease occurs, which makes the disease resistance of Hu sheep stronger under the same disease conditions. However, the enrichment of harmful microorganisms in East Friesian sheep activated the TNFα signalling pathway, which aggravated the intestinal injury, and then the treatment of FMT mice by culturing Roseburia bacteria found that Roseburia bacteria had a good curative effect on colitis.</p><p><strong>Conclusion: </strong>Our study showed that in H-DSS-treated sheep, the intestinal barrier is stabilized with an increase in the abundance of beneficial microorganisms. Our data also suggest that Roseburia bacteria have a protective effect on the intestinal barrier of Hu sheep. Accumulating evidence suggests that host-microbiota interactions are associated with IBD disease progression. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"208"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492479/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469533","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-21DOI: 10.1186/s40168-024-01934-6
Tong Wang, Nannan Zhou, Feifei Ding, Zhenzhen Hao, Jorge Galindo-Villegas, Zhenyu Du, Xiaoyun Su, Meiling Zhang
Background: Commensal bacteria in the intestine release enzymes to degrade and ferment dietary components, producing beneficial metabolites. However, the regulatory effects of microbial-derived enzymes on the intestinal microbiota composition and the influence on host health remain elusive. Xylanase can degrade xylan into oligosaccharides, showing wide application in feed industry.
Results: To validate the immune-protective effects of xylanase, Nile tilapia was used as the model and fed with xylanase. The results showed that dietary xylanase improved the survival rate of Nile tilapia when they were challenged with Aeromonas hydrophila. The transcriptome analysis showed significant enrichment of genes related to interleukin-17d (il-17d) signaling pathway in the xylanase treatment group. High-throughput sequencing revealed that dietary xylanase altered the composition of the intestinal microbiota and directly promoted the proliferation of Allobaculum stercoricanis which could produce butyrate in vitro. Consequently, dietary xylanase supplementation increased the butyrate level in fish gut. Further experiment verified that butyrate supplementation enhanced the expression of il-17d and regenerating islet-derived 3 gamma (reg3g) in the gut. The knockdown experiment of il-17d confirmed that il-17d is necessary for butyrate to protect Nile tilapia from pathogen resistance. Flow cytometry analysis indicated that butyrate increased the abundance of IL-17D+ intestinal epithelial cells in fish. Mechanistically, butyrate functions as an HDAC3 inhibitor, enhancing il-17d expression and playing a crucial role in pathogen resistance.
Conclusion: Dietary xylanase significantly altered the composition of intestinal microbiota and increased the content of butyrate in the intestine. Butyrate activated the transcription of il-17d in intestinal epithelial cells by inhibiting histone deacetylase 3, thereby protecting the Nile tilapia from pathogen infection. This study elucidated how microbial-derived xylanase regulates host immune function, providing a theoretical basis for the development and application of functional enzymes. Video Abstract.
{"title":"Xylanase enhances gut microbiota-derived butyrate to exert immune-protective effects in a histone deacetylase-dependent manner.","authors":"Tong Wang, Nannan Zhou, Feifei Ding, Zhenzhen Hao, Jorge Galindo-Villegas, Zhenyu Du, Xiaoyun Su, Meiling Zhang","doi":"10.1186/s40168-024-01934-6","DOIUrl":"10.1186/s40168-024-01934-6","url":null,"abstract":"<p><strong>Background: </strong>Commensal bacteria in the intestine release enzymes to degrade and ferment dietary components, producing beneficial metabolites. However, the regulatory effects of microbial-derived enzymes on the intestinal microbiota composition and the influence on host health remain elusive. Xylanase can degrade xylan into oligosaccharides, showing wide application in feed industry.</p><p><strong>Results: </strong>To validate the immune-protective effects of xylanase, Nile tilapia was used as the model and fed with xylanase. The results showed that dietary xylanase improved the survival rate of Nile tilapia when they were challenged with Aeromonas hydrophila. The transcriptome analysis showed significant enrichment of genes related to interleukin-17d (il-17d) signaling pathway in the xylanase treatment group. High-throughput sequencing revealed that dietary xylanase altered the composition of the intestinal microbiota and directly promoted the proliferation of Allobaculum stercoricanis which could produce butyrate in vitro. Consequently, dietary xylanase supplementation increased the butyrate level in fish gut. Further experiment verified that butyrate supplementation enhanced the expression of il-17d and regenerating islet-derived 3 gamma (reg3g) in the gut. The knockdown experiment of il-17d confirmed that il-17d is necessary for butyrate to protect Nile tilapia from pathogen resistance. Flow cytometry analysis indicated that butyrate increased the abundance of IL-17D<sup>+</sup> intestinal epithelial cells in fish. Mechanistically, butyrate functions as an HDAC3 inhibitor, enhancing il-17d expression and playing a crucial role in pathogen resistance.</p><p><strong>Conclusion: </strong>Dietary xylanase significantly altered the composition of intestinal microbiota and increased the content of butyrate in the intestine. Butyrate activated the transcription of il-17d in intestinal epithelial cells by inhibiting histone deacetylase 3, thereby protecting the Nile tilapia from pathogen infection. This study elucidated how microbial-derived xylanase regulates host immune function, providing a theoretical basis for the development and application of functional enzymes. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"212"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492574/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469623","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-21DOI: 10.1186/s40168-024-01918-6
Ciara Keating, Elizabeth Kilbride, Mark A Stalham, Charlotte Nellist, Joel Milner, Sonia Humphris, Ian Toth, Barbara K Mable, Umer Zeeshan Ijaz
Background: Understanding the interaction between environmental conditions, crop yields, and soil health is crucial for sustainable agriculture in a changing climate. Management practices to limit disease are a balancing act. For example, in potato production, dry conditions favour common scab (Streptomyces spp.) and wet conditions favour blackleg disease (Pectobacterium spp.). The exact mechanisms involved and how these link to changes in the soil microbiome are unclear. Our objectives were to test how irrigation management and bacterial pathogen load in potato seed stocks impact: (i) crop yields; (ii) disease development (blackleg or common scab); and (iii) soil microbial community dynamics.
Methods: We used stocks of seed potatoes with varying natural levels of Pectobacterium (Jelly [high load], Jelly [low load] and Estima [Zero - no Pectobacterium]). Stocks were grown under four irrigation regimes that differed in the timing and level of watering. The soil microbial communities were profiled using amplicon sequencing at 50% plant emergence and at harvest. Generalised linear latent variable models and an annotation-free mathematical framework approach (ensemble quotient analysis) were then used to show the interacting microbes with irrigation regime and Pectobacterium pathogen levels.
Results: Irrigation increased blackleg symptoms in the plots planted with stocks with low and high levels of Pectobacterium (22-34%) but not in the zero stock (2-6%). However, withholding irrigation increased common scab symptoms (2-5%) and reduced crop yields. Irrigation did not impact the composition of the soil microbiome, but planting stock with a high Pectobacterium burden resulted in an increased abundance of Planctomycetota, Anaerolinea and Acidobacteria species within the microbiome. Ensemble quotient analysis highlighted the Anaerolinea taxa were highly associated with high levels of Pectobacterium in the seed stock and blackleg symptoms in the field.
Conclusions: We conclude that planting seed stocks with a high Pectobacterium burden alters the abundance of specific microbial species within the soil microbiome and suggest that managing pathogen load in seed stocks could substantially affect soil communities, affecting crop health and productivity. Video Abstract.
{"title":"Balancing the scales: assessing the impact of irrigation and pathogen burden on potato blackleg disease and soil microbial communities.","authors":"Ciara Keating, Elizabeth Kilbride, Mark A Stalham, Charlotte Nellist, Joel Milner, Sonia Humphris, Ian Toth, Barbara K Mable, Umer Zeeshan Ijaz","doi":"10.1186/s40168-024-01918-6","DOIUrl":"10.1186/s40168-024-01918-6","url":null,"abstract":"<p><strong>Background: </strong>Understanding the interaction between environmental conditions, crop yields, and soil health is crucial for sustainable agriculture in a changing climate. Management practices to limit disease are a balancing act. For example, in potato production, dry conditions favour common scab (Streptomyces spp.) and wet conditions favour blackleg disease (Pectobacterium spp.). The exact mechanisms involved and how these link to changes in the soil microbiome are unclear. Our objectives were to test how irrigation management and bacterial pathogen load in potato seed stocks impact: (i) crop yields; (ii) disease development (blackleg or common scab); and (iii) soil microbial community dynamics.</p><p><strong>Methods: </strong>We used stocks of seed potatoes with varying natural levels of Pectobacterium (Jelly [high load], Jelly [low load] and Estima [Zero - no Pectobacterium]). Stocks were grown under four irrigation regimes that differed in the timing and level of watering. The soil microbial communities were profiled using amplicon sequencing at 50% plant emergence and at harvest. Generalised linear latent variable models and an annotation-free mathematical framework approach (ensemble quotient analysis) were then used to show the interacting microbes with irrigation regime and Pectobacterium pathogen levels.</p><p><strong>Results: </strong>Irrigation increased blackleg symptoms in the plots planted with stocks with low and high levels of Pectobacterium (22-34%) but not in the zero stock (2-6%). However, withholding irrigation increased common scab symptoms (2-5%) and reduced crop yields. Irrigation did not impact the composition of the soil microbiome, but planting stock with a high Pectobacterium burden resulted in an increased abundance of Planctomycetota, Anaerolinea and Acidobacteria species within the microbiome. Ensemble quotient analysis highlighted the Anaerolinea taxa were highly associated with high levels of Pectobacterium in the seed stock and blackleg symptoms in the field.</p><p><strong>Conclusions: </strong>We conclude that planting seed stocks with a high Pectobacterium burden alters the abundance of specific microbial species within the soil microbiome and suggest that managing pathogen load in seed stocks could substantially affect soil communities, affecting crop health and productivity. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"210"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492761/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469530","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-21DOI: 10.1186/s40168-024-01923-9
Merel van Gogh, Jonas M Louwers, Anna Celli, Sanne Gräve, Marco C Viveen, Sofie Bosch, Nanne K H de Boer, Rik J Verheijden, Karijn P M Suijkerbuijk, Eelco C Brand, Janetta Top, Bas Oldenburg, Marcel R de Zoete
Background: The intestinal microbiota plays a significant role in maintaining systemic and intestinal homeostasis, but can also influence diseases such as inflammatory bowel disease (IBD) and cancer. Certain bacterial species within the intestinal tract can chronically activate the immune system, leading to low-grade intestinal inflammation. As a result, plasma cells produce high levels of secretory antigen-specific immunoglobulin A (IgA), which coats the immunostimulatory bacteria. This IgA immune response against intestinal bacteria may be associated with the maintenance of homeostasis and health, as well as disease. Unraveling this dichotomy and identifying the immunostimulatory bacteria is crucial for understanding the relationship between the intestinal microbiota and the immune system, and their role in health and disease. IgA-SEQ technology has successfully identified immunostimulatory, IgA-coated bacteria from fecal material. However, the original technology is time-consuming and has limited downstream applications. In this study, we aimed to develop a next-generation, high-throughput, magnet-based sorting approach (ng-IgA-SEQ) to overcome the limitations of the original IgA-SEQ protocol.
Results: We show, in various settings of complexity ranging from simple bacterial mixtures to human fecal samples, that our magnetic 96-well plate-based ng-IgA-SEQ protocol is highly efficient at sorting and identifying IgA-coated bacteria in a high-throughput and time efficient manner. Furthermore, we performed a comparative analysis between different IgA-SEQ protocols, highlighting that the original FACS-based IgA-SEQ approach overlooks certain nuances of IgA-coated bacteria, due to the low yield of sorted bacteria. Additionally, magnetic-based ng-IgA-SEQ allows for novel downstream applications. Firstly, as a proof-of-concept, we performed metagenomic shotgun sequencing on 10 human fecal samples to identify IgA-coated bacterial strains and associated pathways and CAZymes. Secondly, we successfully isolated and cultured IgA-coated bacteria by performing the isolation protocol under anaerobic conditions.
Conclusions: Our magnetic 96-well plate-based high-throughput next-generation IgA-SEQ technology efficiently identifies a great number of IgA-coated bacteria from fecal samples. This paves the way for analyzing large cohorts as well as novel downstream applications, including shotgun metagenomic sequencing, culturomics, and various functional assays. These downstream applications are essential to unravel the role of immunostimulatory bacteria in health and disease. Video Abstract.
背景:肠道微生物群在维持全身和肠道平衡方面发挥着重要作用,但也会影响炎症性肠病(IBD)和癌症等疾病。肠道内的某些细菌可长期激活免疫系统,导致低度肠道炎症。因此,浆细胞会产生大量分泌性抗原特异性免疫球蛋白 A(IgA),包裹住免疫刺激细菌。这种针对肠道细菌的 IgA 免疫反应可能与维持平衡和健康以及疾病有关。要了解肠道微生物群与免疫系统之间的关系以及它们在健康和疾病中的作用,揭示这种二分法并确定免疫刺激细菌至关重要。IgA-SEQ 技术已成功地从粪便材料中鉴定出了具有免疫刺激作用的 IgA 包被细菌。然而,原始技术耗时长,下游应用有限。在本研究中,我们旨在开发一种下一代、高通量、基于磁铁的分选方法(ng-IgA-SEQ),以克服原始 IgA-SEQ 方案的局限性:结果:我们在从简单的细菌混合物到人类粪便样本的各种复杂环境中表明,我们基于磁性 96 孔板的 ng-IgA-SEQ 方案能以高通量和省时的方式高效分拣和鉴定 IgA 包被细菌。此外,我们还对不同的 IgA-SEQ 方案进行了比较分析,结果表明,最初基于 FACS 的 IgA-SEQ 方法由于分选细菌的产量较低而忽略了 IgA 包被细菌的某些细微差别。此外,基于磁性的 ng-IgA-SEQ 还可用于新型下游应用。首先,作为概念验证,我们对 10 份人类粪便样本进行了元基因组枪式测序,以确定 IgA 包被细菌菌株及相关途径和 CAZymes。其次,我们通过在厌氧条件下执行分离方案,成功分离并培养了IgA包被菌:结论:我们基于磁性 96 孔板的高通量新一代 IgA-SEQ 技术能从粪便样本中有效鉴定出大量 IgA 包被菌。这为分析大型群体以及新型下游应用(包括散弹枪元基因组测序、培养组学和各种功能测定)铺平了道路。这些下游应用对于揭示免疫刺激细菌在健康和疾病中的作用至关重要。视频摘要。
{"title":"Next-generation IgA-SEQ allows for high-throughput, anaerobic, and metagenomic assessment of IgA-coated bacteria.","authors":"Merel van Gogh, Jonas M Louwers, Anna Celli, Sanne Gräve, Marco C Viveen, Sofie Bosch, Nanne K H de Boer, Rik J Verheijden, Karijn P M Suijkerbuijk, Eelco C Brand, Janetta Top, Bas Oldenburg, Marcel R de Zoete","doi":"10.1186/s40168-024-01923-9","DOIUrl":"10.1186/s40168-024-01923-9","url":null,"abstract":"<p><strong>Background: </strong>The intestinal microbiota plays a significant role in maintaining systemic and intestinal homeostasis, but can also influence diseases such as inflammatory bowel disease (IBD) and cancer. Certain bacterial species within the intestinal tract can chronically activate the immune system, leading to low-grade intestinal inflammation. As a result, plasma cells produce high levels of secretory antigen-specific immunoglobulin A (IgA), which coats the immunostimulatory bacteria. This IgA immune response against intestinal bacteria may be associated with the maintenance of homeostasis and health, as well as disease. Unraveling this dichotomy and identifying the immunostimulatory bacteria is crucial for understanding the relationship between the intestinal microbiota and the immune system, and their role in health and disease. IgA-SEQ technology has successfully identified immunostimulatory, IgA-coated bacteria from fecal material. However, the original technology is time-consuming and has limited downstream applications. In this study, we aimed to develop a next-generation, high-throughput, magnet-based sorting approach (ng-IgA-SEQ) to overcome the limitations of the original IgA-SEQ protocol.</p><p><strong>Results: </strong>We show, in various settings of complexity ranging from simple bacterial mixtures to human fecal samples, that our magnetic 96-well plate-based ng-IgA-SEQ protocol is highly efficient at sorting and identifying IgA-coated bacteria in a high-throughput and time efficient manner. Furthermore, we performed a comparative analysis between different IgA-SEQ protocols, highlighting that the original FACS-based IgA-SEQ approach overlooks certain nuances of IgA-coated bacteria, due to the low yield of sorted bacteria. Additionally, magnetic-based ng-IgA-SEQ allows for novel downstream applications. Firstly, as a proof-of-concept, we performed metagenomic shotgun sequencing on 10 human fecal samples to identify IgA-coated bacterial strains and associated pathways and CAZymes. Secondly, we successfully isolated and cultured IgA-coated bacteria by performing the isolation protocol under anaerobic conditions.</p><p><strong>Conclusions: </strong>Our magnetic 96-well plate-based high-throughput next-generation IgA-SEQ technology efficiently identifies a great number of IgA-coated bacteria from fecal samples. This paves the way for analyzing large cohorts as well as novel downstream applications, including shotgun metagenomic sequencing, culturomics, and various functional assays. These downstream applications are essential to unravel the role of immunostimulatory bacteria in health and disease. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"211"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492651/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469617","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Background: The ecosystems of marine ranching have enhanced marine biodiversity and ecological balance and have promoted the natural recovery and enhancement of fishery resources. The microbial communities of these ecosystems, including bacteria, fungi, protists, and viruses, are the drivers of biogeochemical cycles. Although seasonal changes in microbial communities are critical for ecosystem functioning, the current understanding of microbial-driven metabolic properties and their viral communities in marine sediments remains limited. Here, we employed amplicon (16S and 18S) and metagenomic approaches aiming to reveal the seasonal patterns of microbial communities, bacterial-eukaryotic interactions, whole metabolic potential, and their coupling mechanisms with carbon (C), nitrogen (N), and sulfur (S) cycling in marine ranching sediments. Additionally, the characterization and diversity of viral communities in different seasons were explored in marine ranching sediments.
Results: The current study demonstrated that seasonal variations dramatically affected the diversity of microbial communities in marine ranching sediments and the bacterial-eukaryotic interkingdom co-occurrence networks. Metabolic reconstruction of the 113 medium to high-quality metagenome-assembled genomes (MAGs) was conducted, and a total of 8 MAGs involved in key metabolic genes and pathways (methane oxidation - denitrification - S oxidation), suggesting a possible coupling effect between the C, N, and S cycles. In total, 338 viral operational taxonomic units (vOTUs) were identified, all possessing specific ecological characteristics in different seasons and primarily belonging to Caudoviricetes, revealing their widespread distribution and variety in marine sediment ecosystems. In addition, predicted virus-host linkages showed that high host specificity was observed, with few viruses associated with specific hosts.
Conclusions: This finding deepens our knowledge of element cycling and viral diversity in fisheries enrichment ecosystems, providing insights into microbial-virus interactions in marine sediments and their effects on biogeochemical cycling. These findings have potential applications in marine ranching management and ecological conservation. Video Abstract.
{"title":"Seasonal variations of microbial communities and viral diversity in fishery-enhanced marine ranching sediments: insights into metabolic potentials and ecological interactions.","authors":"Cheng-Zhuang Chen, Ping Li, Ling Liu, Yong-Jun Sun, Wen-Ming Ju, Zhi-Hua Li","doi":"10.1186/s40168-024-01922-w","DOIUrl":"10.1186/s40168-024-01922-w","url":null,"abstract":"<p><strong>Background: </strong>The ecosystems of marine ranching have enhanced marine biodiversity and ecological balance and have promoted the natural recovery and enhancement of fishery resources. The microbial communities of these ecosystems, including bacteria, fungi, protists, and viruses, are the drivers of biogeochemical cycles. Although seasonal changes in microbial communities are critical for ecosystem functioning, the current understanding of microbial-driven metabolic properties and their viral communities in marine sediments remains limited. Here, we employed amplicon (16S and 18S) and metagenomic approaches aiming to reveal the seasonal patterns of microbial communities, bacterial-eukaryotic interactions, whole metabolic potential, and their coupling mechanisms with carbon (C), nitrogen (N), and sulfur (S) cycling in marine ranching sediments. Additionally, the characterization and diversity of viral communities in different seasons were explored in marine ranching sediments.</p><p><strong>Results: </strong>The current study demonstrated that seasonal variations dramatically affected the diversity of microbial communities in marine ranching sediments and the bacterial-eukaryotic interkingdom co-occurrence networks. Metabolic reconstruction of the 113 medium to high-quality metagenome-assembled genomes (MAGs) was conducted, and a total of 8 MAGs involved in key metabolic genes and pathways (methane oxidation - denitrification - S oxidation), suggesting a possible coupling effect between the C, N, and S cycles. In total, 338 viral operational taxonomic units (vOTUs) were identified, all possessing specific ecological characteristics in different seasons and primarily belonging to Caudoviricetes, revealing their widespread distribution and variety in marine sediment ecosystems. In addition, predicted virus-host linkages showed that high host specificity was observed, with few viruses associated with specific hosts.</p><p><strong>Conclusions: </strong>This finding deepens our knowledge of element cycling and viral diversity in fisheries enrichment ecosystems, providing insights into microbial-virus interactions in marine sediments and their effects on biogeochemical cycling. These findings have potential applications in marine ranching management and ecological conservation. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"209"},"PeriodicalIF":13.8,"publicationDate":"2024-10-21","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11492486/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469618","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-18DOI: 10.1186/s40168-024-01940-8
Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie
Background: Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.
Results: We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.
Conclusions: In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.
{"title":"Upper respiratory microbial communities of healthy populations are shaped by niche and age.","authors":"Susan Zelasko, Mary Hannah Swaney, Shelby Sandstrom, Timothy C Davenport, Christine M Seroogy, James E Gern, Lindsay R Kalan, Cameron R Currie","doi":"10.1186/s40168-024-01940-8","DOIUrl":"10.1186/s40168-024-01940-8","url":null,"abstract":"<p><strong>Background: </strong>Alterations in upper respiratory microbiomes have been implicated in shaping host health trajectories, including by limiting mucosal pathogen colonization. However, limited comparative studies of respiratory microbiome development and functioning across age groups have been performed. Herein, we perform shotgun metagenomic sequencing paired with pathogen inhibition assays to elucidate differences in nasal and oral microbiome composition and intermicrobial interactions across healthy 24-month-old infant (n = 229) and adult (n = 100) populations.</p><p><strong>Results: </strong>We find that beta diversity of nasal and oral microbiomes varies with age, with nasal microbiomes showing greater population-level variation compared to oral microbiomes. Infant microbiome alpha diversity was significantly lower across nasal samples and higher in oral samples, relative to adults. Accordingly, we demonstrate significant differences in genus- and species-level composition of microbiomes between sites and age groups. Antimicrobial resistome patterns likewise varied across body sites, with oral microbiomes showing higher resistance gene abundance compared to nasal microbiomes. Biosynthetic gene clusters encoding specialized metabolite production were found in higher abundance across infant oral microbiomes, relative to adults. Investigation of pathogen inhibition revealed greater inhibition of gram-negative and gram-positive bacteria by oral commensals, while nasal isolates had higher antifungal activity.</p><p><strong>Conclusions: </strong>In summary, we identify significant differences in the microbial communities inhabiting nasal and oral cavities of healthy infants relative to adults. These findings inform our understanding of the interactions impacting respiratory microbiome composition and functions related to colonization resistance, with important implications for host health across the lifespan. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"206"},"PeriodicalIF":13.8,"publicationDate":"2024-10-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11490146/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469620","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-10-17DOI: 10.1186/s40168-024-01899-6
Abeeha Khalil, Anna R Bramucci, Amaranta Focardi, Nine Le Reun, Nathan L R Willams, Unnikrishnan Kuzhiumparambil, Jean-Baptiste Raina, Justin R Seymour
Background: Reciprocal exchanges of metabolites between phytoplankton and bacteria influence the fitness of these microorganisms which ultimately shapes the productivity of marine ecosystems. Recent evidence suggests that plant growth-promoting hormones may be key metabolites within mutualistic phytoplankton-bacteria partnerships, but very little is known about the diversity of plant growth-promoting hormones produced by marine bacteria and their specific effects on phytoplankton growth. Here, we aimed to investigate the capacity of marine bacteria to produce 7 plant growth-promoting hormones and the effects of these hormones on Actinocyclus sp. growth.
Results: We examined the plant growth-promoting hormone synthesis capabilities of 14 bacterial strains that enhance the growth of the common diatom Actinocyclus. Plant growth-promoting hormone biosynthesis was ubiquitous among the bacteria tested. Indeed all 14 strains displayed the genomic potential to synthesise multiple hormones, and mass-spectrometry confirmed that each strain produced at least 6 out of the 7 tested plant growth-promoting hormones. Some of the plant growth-promoting hormones identified here, such as brassinolide and trans-zeatin, have never been reported in marine microorganisms. Importantly, all strains produced the hormone indole-3 acetic acid (IAA) in high concentrations and released it into their surroundings. Furthermore, indole-3 acetic acid extracellular concentrations were positively correlated with the ability of each strain to promote Actinocyclus growth. When inoculated with axenic Actinocyclus cultures, only indole-3 acetic acid and gibberellic acid enhanced the growth of the diatom, with cultures exposed to indole-3 acetic acid exhibiting a two-fold increase in cell numbers.
Conclusion: Our results reveal that marine bacteria produce a much broader range of plant growth-promoting hormones than previously suspected and that some of these compounds enhance the growth of a marine diatom. These findings suggest plant growth-promoting hormones play a large role in microbial communication and broaden our knowledge of their fuctions in the marine environment. Video Abstract.
{"title":"Widespread production of plant growth-promoting hormones among marine bacteria and their impacts on the growth of a marine diatom.","authors":"Abeeha Khalil, Anna R Bramucci, Amaranta Focardi, Nine Le Reun, Nathan L R Willams, Unnikrishnan Kuzhiumparambil, Jean-Baptiste Raina, Justin R Seymour","doi":"10.1186/s40168-024-01899-6","DOIUrl":"https://doi.org/10.1186/s40168-024-01899-6","url":null,"abstract":"<p><strong>Background: </strong>Reciprocal exchanges of metabolites between phytoplankton and bacteria influence the fitness of these microorganisms which ultimately shapes the productivity of marine ecosystems. Recent evidence suggests that plant growth-promoting hormones may be key metabolites within mutualistic phytoplankton-bacteria partnerships, but very little is known about the diversity of plant growth-promoting hormones produced by marine bacteria and their specific effects on phytoplankton growth. Here, we aimed to investigate the capacity of marine bacteria to produce 7 plant growth-promoting hormones and the effects of these hormones on Actinocyclus sp. growth.</p><p><strong>Results: </strong>We examined the plant growth-promoting hormone synthesis capabilities of 14 bacterial strains that enhance the growth of the common diatom Actinocyclus. Plant growth-promoting hormone biosynthesis was ubiquitous among the bacteria tested. Indeed all 14 strains displayed the genomic potential to synthesise multiple hormones, and mass-spectrometry confirmed that each strain produced at least 6 out of the 7 tested plant growth-promoting hormones. Some of the plant growth-promoting hormones identified here, such as brassinolide and trans-zeatin, have never been reported in marine microorganisms. Importantly, all strains produced the hormone indole-3 acetic acid (IAA) in high concentrations and released it into their surroundings. Furthermore, indole-3 acetic acid extracellular concentrations were positively correlated with the ability of each strain to promote Actinocyclus growth. When inoculated with axenic Actinocyclus cultures, only indole-3 acetic acid and gibberellic acid enhanced the growth of the diatom, with cultures exposed to indole-3 acetic acid exhibiting a two-fold increase in cell numbers.</p><p><strong>Conclusion: </strong>Our results reveal that marine bacteria produce a much broader range of plant growth-promoting hormones than previously suspected and that some of these compounds enhance the growth of a marine diatom. These findings suggest plant growth-promoting hormones play a large role in microbial communication and broaden our knowledge of their fuctions in the marine environment. Video Abstract.</p>","PeriodicalId":18447,"journal":{"name":"Microbiome","volume":"12 1","pages":"205"},"PeriodicalIF":13.8,"publicationDate":"2024-10-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11487934/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142469622","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}