Bacterial endosymbionts of a nitrogen-fixing yeast Rhodotorula mucilaginosa JGTA-S1 – insights into a yet unknown micro-ecosystem

IF 3 4区 生物学 Q3 BIOCHEMISTRY & MOLECULAR BIOLOGY
Molecular omics Pub Date : 2024-08-28 DOI:10.1039/d3mo00273j
Mayurakshi Nag, Janardhan Pallavi, Sandipan Chakraborty, Trina Roychoudhury, Sangita Mondal, Abhrajyoti Ghosh, Chinmay Saha, Manidipa Banerjee, Anindita Seal
{"title":"Bacterial endosymbionts of a nitrogen-fixing yeast Rhodotorula mucilaginosa JGTA-S1 – insights into a yet unknown micro-ecosystem","authors":"Mayurakshi Nag, Janardhan Pallavi, Sandipan Chakraborty, Trina Roychoudhury, Sangita Mondal, Abhrajyoti Ghosh, Chinmay Saha, Manidipa Banerjee, Anindita Seal","doi":"10.1039/d3mo00273j","DOIUrl":null,"url":null,"abstract":"<em>Rhodotorula mucilaginosa</em> JGTA-S1 is a yeast strain capable of fixing nitrogen and improving nitrogen nutrition in rice plants because of its nitrogen-fixing endobacteria, namely <em>Stutzerimonas</em> (<em>Pseudomonas</em>) <em>stutzeri</em> and <em>Bradyrhizobium</em> sp. To gain a deeper understanding of yeast endosymbionts, we conducted a whole-genome shotgun metagenomic analysis of JGTA-S1 cells grown under conditions of nitrogen sufficiency and deficiency. Our results showed that the endosymbiont population varied depending on the nitrogen regime. Upon mechanical disruption of yeast cells, we obtained endosymbionts in culturable form <em>viz. Bacillus velezensis</em> and <em>Staphylococcus</em> sp. under nitrogen-replete conditions and <em>Lysinibacillus telephonicus.</em>, <em>Brevibacillus</em> sp., and <em>Niallia circulans</em> under nitrogen-depleted conditions. <em>S. stutzeri</em> and <em>Bradyrhizobium</em> sp. the previously reported endosymbionts remained unculturable. The culturable endosymbionts <em>Staphylococcus</em> sp. and <em>Bacillus velezensis</em> appear to possess genes for dissimilatory nitrate reduction (DNRA), an alternative pathway for ammonia synthesis. However, our findings suggest that these endosymbionts are facultative as they survive outside the host. The fitness of the yeast was not affected by curing of these microbes. Curing the yeast diazotrophic endosymbionts took a toll on its fitness. Our results also showed that the populations of <em>S. stutzeri</em> and <em>B. velezensis</em> increased significantly under nitrogen-depleted conditions compared to nitrogen-sufficient conditions. The importance of DNRA and nitrogen fixation is also reflected in the metagenomic reads of JGTA-S1.","PeriodicalId":19065,"journal":{"name":"Molecular omics","volume":null,"pages":null},"PeriodicalIF":3.0000,"publicationDate":"2024-08-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Molecular omics","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1039/d3mo00273j","RegionNum":4,"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

Abstract

Rhodotorula mucilaginosa JGTA-S1 is a yeast strain capable of fixing nitrogen and improving nitrogen nutrition in rice plants because of its nitrogen-fixing endobacteria, namely Stutzerimonas (Pseudomonas) stutzeri and Bradyrhizobium sp. To gain a deeper understanding of yeast endosymbionts, we conducted a whole-genome shotgun metagenomic analysis of JGTA-S1 cells grown under conditions of nitrogen sufficiency and deficiency. Our results showed that the endosymbiont population varied depending on the nitrogen regime. Upon mechanical disruption of yeast cells, we obtained endosymbionts in culturable form viz. Bacillus velezensis and Staphylococcus sp. under nitrogen-replete conditions and Lysinibacillus telephonicus., Brevibacillus sp., and Niallia circulans under nitrogen-depleted conditions. S. stutzeri and Bradyrhizobium sp. the previously reported endosymbionts remained unculturable. The culturable endosymbionts Staphylococcus sp. and Bacillus velezensis appear to possess genes for dissimilatory nitrate reduction (DNRA), an alternative pathway for ammonia synthesis. However, our findings suggest that these endosymbionts are facultative as they survive outside the host. The fitness of the yeast was not affected by curing of these microbes. Curing the yeast diazotrophic endosymbionts took a toll on its fitness. Our results also showed that the populations of S. stutzeri and B. velezensis increased significantly under nitrogen-depleted conditions compared to nitrogen-sufficient conditions. The importance of DNRA and nitrogen fixation is also reflected in the metagenomic reads of JGTA-S1.

Abstract Image

固氮酵母 Rhodotorula mucilaginosa JGTA-S1 的细菌内共生体--洞察一个未知的微生态系统
为了更深入地了解酵母内共生菌,我们对在氮充足和氮缺乏条件下生长的 JGTA-S1 细胞进行了全基因组霰弹枪元基因组分析。我们的结果表明,内共生菌的数量随氮浓度的变化而变化。在机械破坏酵母细胞后,我们获得了可培养的内共生菌,即在氮充足条件下的韦氏芽孢杆菌(Bacillus velezensis)和葡萄球菌(Staphylococcus sp.),以及在氮缺乏条件下的远程溶菌酶(Lysinibacillus telephonicus.)、布拉维杆菌(Brevibacillus sp.)和Niallia circulans。之前报道的内生共生菌 S. stutzeri 和 Bradyrhizobium sp.可培养的内生菌葡萄球菌(Staphylococcus sp.不过,我们的研究结果表明,这些内共生菌是面生的,因为它们在宿主之外生存。这些微生物的固化不会影响酵母的适应性。酵母重氮内共生菌的固化对其适应性有影响。我们的研究结果还表明,与氮充足的条件相比,缺氮条件下 S. stutzeri 和 B. velezensis 的数量显著增加。JGTA-S1 的元基因组读数也反映了 DNRA 和固氮的重要性。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
来源期刊
Molecular omics
Molecular omics Biochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
5.40
自引率
3.40%
发文量
91
期刊介绍: Molecular Omics publishes high-quality research from across the -omics sciences. Topics include, but are not limited to: -omics studies to gain mechanistic insight into biological processes – for example, determining the mode of action of a drug or the basis of a particular phenotype, such as drought tolerance -omics studies for clinical applications with validation, such as finding biomarkers for diagnostics or potential new drug targets -omics studies looking at the sub-cellular make-up of cells – for example, the subcellular localisation of certain proteins or post-translational modifications or new imaging techniques -studies presenting new methods and tools to support omics studies, including new spectroscopic/chromatographic techniques, chip-based/array technologies and new classification/data analysis techniques. New methods should be proven and demonstrate an advance in the field. Molecular Omics only accepts articles of high importance and interest that provide significant new insight into important chemical or biological problems. This could be fundamental research that significantly increases understanding or research that demonstrates clear functional benefits. Papers reporting new results that could be routinely predicted, do not show a significant improvement over known research, or are of interest only to the specialist in the area are not suitable for publication in Molecular Omics.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
联系我们:info@booksci.cn Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。 Copyright © 2023 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信