Sinorhizobium sp.NGR234的广宿主适应机制研究
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摘要
根瘤菌与豆科植物互作最特殊之处就是形成固氮器官-根瘤,根瘤按照持续分生组织的有无分为无限根瘤和有限根瘤。根瘤菌对两种根瘤适应机制的比较研究是根瘤菌-豆科植物共生的研究热点。由于根瘤菌有很强的宿主选择性,一直以来对于根瘤菌适应这两种根瘤的系统研究都是基于不同根瘤菌和不同宿主,菌株间遗传背景的筹异使得相关的比较分析困难重重。本论文选取广宿主根瘤菌Sinorhizobium sp. NGR234与无限根瘤宿主(银合欢,Leucaena leucocephala)和有限根瘤宿主(豇豆,Vigna unguiculata)为材料研究同一株根瘤菌对两种根瘤的适应机制。通过对NGR234在银合欢、豇豆根瘤中形成的类菌体进行链特异性RNA-seq比较转录组学研究,从全局上揭示根瘤菌对无限根瘤和有限根瘤的适应机制,进而通过遗传学手段研究相关差异表达基因在共生过程中的作用,逐步揭示根瘤菌适应无限根瘤和有限根瘤机制的异同。
以对数生长期的纯培养根瘤菌Sinorhizobium sp. NGR234为参照,对该菌株在两种根瘤中形成的类菌体进行了基于链特异性RNA-seq的比较转录组学研究。结果发现：1)相对于纯培养根瘤菌,在类菌体中两个质粒上的基因表达上调显著,但染色体上的基因下调显著；2)两种根瘤中的类菌体的以下一些编码基因都表达上调,如细胞色素cbb3氧化酶、硫胺素合成、硝酸盐还原途径(产生NO)、琥珀酸代谢途径、PHB(聚-β-羟基丁酸)合成和磷酸/磷酸盐转运途径；3)两种根瘤中的类菌体在以下一些相关编码基因的表达有显著差异,EPS (Exopolysaccharides)、LPS (Lipopolysaccharides)、T3SS(Ⅲ型分泌系统)及其效应蛋白、细胞色素bd泛醌氧化酶、PQQ (Pyrroloquinoline quinone)、细胞色素c550、假天青蛋白、生物素、phasins、乙醇酸氧化酶、谷氨酸和苯丙氨酸代谢等。
基于上述转录组数据,构建了19个差异表达基因的删除突变株。其中9个突变株与豇豆共生时,类菌体发育不止常：分别编码Phasin1、Phasin3, ATP-dependent carboxylate-amine ligase, Hypothetical protein, PRC-barrel domain protein, UspA, Cytochrome bd-11, RibH。而这9个突变体中的5个突变体不能止常侵染木豆(Cajanus cajan);4个突变体不能止常侵染扁豆(Lablab purpureus),1个突变体在扁豆根瘤中的类菌体发育不正常。而绝大部分突变体(18/19)与银合欢的共生能力和野生型菌株均无显著性差异,或许是银合欢能够为其无限根瘤中的根瘤菌提供更丰富的碳源或能源物质,即使根瘤菌丧失了上述基因功能,仍然能够进行正常的生物固氮。这四种宿主中,木豆和银合欢形成无限根瘤,而豇豆和扁豆形成有限根瘤。这表明根瘤菌NGR234的同一个基因在与不同宿主共生过程中,同一基因可能影响与不同宿主互作的不同阶段--侵染阶段或类菌体发育阶段,而这种共生表型与根瘤类型无关。
与NGR234基因组系统发育关系较近的根瘤菌都可以与大豆/野大豆(Glycine max/Glycine sojae)共生,但NGR234却不能与大豆/野大豆共生。通过对NGR234进行Tn5突变体库的构建和筛选获得与野大豆共生能力比野生型菌株提高的7株突变体——但结瘤数量少,结瘤表型不稳定。推测NGR234需要多次突变或获得外源基因才能与野大豆建立有效共生关系。在突变体库中筛选到一个LysR转录调控因子编码基因的突变体,能够与木豆、银合欢和豇豆正常结瘤固氮,但侵染原宿主扁豆的能力大大降低,该转录调控因子目前已知的同源蛋白大多存在于病原菌中,这说明NGR234可能使用与这些病原菌类似的机制来侵染扁豆,而这个转录因子编码基因有可能是通过水平基因转移获得的。
The rhizobium-legume interaction is characterized by its ability of forming nitrogen-fixing nodules. Nodules can be categorized into either indeterminate or determinate nodules based on whether a persistent meristem is present or not. The adaptation mechanisms of rhizobium in these two kinds of nodules have been intensively studied. However because of host specificity, most systematic studies in this field were performed on different bacteria and their corresponding hosts. In this study, by using broad host rhizobium Sinorhizobium sp. NGR234and its indeterminate nodule host Leucaena leucocephala and determinate nodule host Vigna unguiculata, we aimed to study the adaptive mechanisms of a rhizobium in these two different nodules. RNA-seq was used to uncover transcriptomic differences between bacteroids in determinate nodules and those in indeterminate nodules. Genetic methods were then used to study the symbiotic role of representatives of differentially expressed genes. This study would provide further insights into the adaptation mechanisms of rhizobium in determinate and indeterminate nodules.
In contrast to exponentially growing free-living bacteria, in bacteroids most genes on two plasmids were significantly up-regulated whereas the majority of chromosomal genes were down-regulated. Bacteroids from two legumes recruited several common cellular functions such as cbb3oxidase, thiamine biosynthesis, nitrate reduction pathway (NO-producing), succinate metabolism, PHB (poly-3-hydroxybutyrate) biosynthesis and phosphate/phosphonate transporters. However, different transcription profiles between bacteroids from two legumes were also uncovered for genes involved in the biosynthesis of exopolysaccharides, lipopolysaccharides, T3SS (type three secretion system) and effector proteins, cytochrome bd ubiquinol oxidase, PQQ (pyrroloquinoline quinone), cytochrome c550, pseudoazurin, biotin, phasins and glycolate oxidase, and in the metabolism of glutamate and phenylalanine.
Based on these transcriptomic results,19deletion mutants were constructed for corresponding differentially expressed genes. Nine mutants showed defects in bacteroids persistance in V. unguiculata nodules and these genes encode Phasin1, Phasin2, ATP-dependent carboxylate-amine ligase, Hypothetical protein, PRC-barrel domain protein, UspA, cytochrome bd-Ⅱ, and RibH respectively. Among these nine mutants, five and four mutants were impaired in infecting nodules of Cajanus cajan and Lablab purpureus, respectively; one mutant showed defects in bacteroids persistence in L. purpureus nodules. However no significant differences were observed between wild type strain and18/19mutants when they were inoculated on L. leucocephala. Thus we hypothesized that, in contrast to V. unguiculata, C. cajan and L. purpureus, L. leucocephala might provide rhizobia with more carbon and energy sources that could support normal symbiotic process when the above mentioned mutants were inoculated. Among these four lemume hosts, L. leucocephala and C. cajan formed indeterminate nodules whereas V. unguiculata and L. purpureus formed determinate nodules. Taken together, these findings suggest that the symbiotic role of the same gene of NGR234showed noticeable variations, when forming symbiosis with different legume hosts, in terms of the essentialbility for different symbiotic stages (infection or bacteroids differentiation). And these symbiotic phenotypes have no correlation with nodule types (indeterminate or determinate nodules).
All strains closely clustered with NGR234in the genome based phylogenetic tree can form nitrogen-fixing nodules with Glycine max/Glycine sojae, whereas NGR234can not. By constructing and screening a Tn5mutant library of NGR234, seven mutants were found to be able to form nitrogen-fixing nodules on G. sojae (1-1.6nodules per plant), though10%-30%of plants inoculated with these seven mutants did not have effective nodules. These results imply that multiple mutation events or some foreign genes might be needed by NGR234for establishing more stable and effective symbiosis with G. sojae. Interestingly, in this mutant library, a mutant of the gene encoding a LysR regulator formed effective nodules on C. cajan, L. leucocephala and V. unguiculata, but was impaired in infecting its primary host L. purpureus. Most homologs of this LysR regulator were present in pathogenic bacteria, indicating that NGR234could use certain mechanism similar to those pathogens to infect L. purpureus and that the coding gene of this regulator could have been laterally transferred to NGR234.
以对数生长期的纯培养根瘤菌Sinorhizobium sp. NGR234为参照,对该菌株在两种根瘤中形成的类菌体进行了基于链特异性RNA-seq的比较转录组学研究。结果发现：1)相对于纯培养根瘤菌,在类菌体中两个质粒上的基因表达上调显著,但染色体上的基因下调显著；2)两种根瘤中的类菌体的以下一些编码基因都表达上调,如细胞色素cbb3氧化酶、硫胺素合成、硝酸盐还原途径(产生NO)、琥珀酸代谢途径、PHB(聚-β-羟基丁酸)合成和磷酸/磷酸盐转运途径；3)两种根瘤中的类菌体在以下一些相关编码基因的表达有显著差异,EPS (Exopolysaccharides)、LPS (Lipopolysaccharides)、T3SS(Ⅲ型分泌系统)及其效应蛋白、细胞色素bd泛醌氧化酶、PQQ (Pyrroloquinoline quinone)、细胞色素c550、假天青蛋白、生物素、phasins、乙醇酸氧化酶、谷氨酸和苯丙氨酸代谢等。
基于上述转录组数据,构建了19个差异表达基因的删除突变株。其中9个突变株与豇豆共生时,类菌体发育不止常：分别编码Phasin1、Phasin3, ATP-dependent carboxylate-amine ligase, Hypothetical protein, PRC-barrel domain protein, UspA, Cytochrome bd-11, RibH。而这9个突变体中的5个突变体不能止常侵染木豆(Cajanus cajan);4个突变体不能止常侵染扁豆(Lablab purpureus),1个突变体在扁豆根瘤中的类菌体发育不正常。而绝大部分突变体(18/19)与银合欢的共生能力和野生型菌株均无显著性差异,或许是银合欢能够为其无限根瘤中的根瘤菌提供更丰富的碳源或能源物质,即使根瘤菌丧失了上述基因功能,仍然能够进行正常的生物固氮。这四种宿主中,木豆和银合欢形成无限根瘤,而豇豆和扁豆形成有限根瘤。这表明根瘤菌NGR234的同一个基因在与不同宿主共生过程中,同一基因可能影响与不同宿主互作的不同阶段--侵染阶段或类菌体发育阶段,而这种共生表型与根瘤类型无关。
与NGR234基因组系统发育关系较近的根瘤菌都可以与大豆/野大豆(Glycine max/Glycine sojae)共生,但NGR234却不能与大豆/野大豆共生。通过对NGR234进行Tn5突变体库的构建和筛选获得与野大豆共生能力比野生型菌株提高的7株突变体——但结瘤数量少,结瘤表型不稳定。推测NGR234需要多次突变或获得外源基因才能与野大豆建立有效共生关系。在突变体库中筛选到一个LysR转录调控因子编码基因的突变体,能够与木豆、银合欢和豇豆正常结瘤固氮,但侵染原宿主扁豆的能力大大降低,该转录调控因子目前已知的同源蛋白大多存在于病原菌中,这说明NGR234可能使用与这些病原菌类似的机制来侵染扁豆,而这个转录因子编码基因有可能是通过水平基因转移获得的。
The rhizobium-legume interaction is characterized by its ability of forming nitrogen-fixing nodules. Nodules can be categorized into either indeterminate or determinate nodules based on whether a persistent meristem is present or not. The adaptation mechanisms of rhizobium in these two kinds of nodules have been intensively studied. However because of host specificity, most systematic studies in this field were performed on different bacteria and their corresponding hosts. In this study, by using broad host rhizobium Sinorhizobium sp. NGR234and its indeterminate nodule host Leucaena leucocephala and determinate nodule host Vigna unguiculata, we aimed to study the adaptive mechanisms of a rhizobium in these two different nodules. RNA-seq was used to uncover transcriptomic differences between bacteroids in determinate nodules and those in indeterminate nodules. Genetic methods were then used to study the symbiotic role of representatives of differentially expressed genes. This study would provide further insights into the adaptation mechanisms of rhizobium in determinate and indeterminate nodules.
In contrast to exponentially growing free-living bacteria, in bacteroids most genes on two plasmids were significantly up-regulated whereas the majority of chromosomal genes were down-regulated. Bacteroids from two legumes recruited several common cellular functions such as cbb3oxidase, thiamine biosynthesis, nitrate reduction pathway (NO-producing), succinate metabolism, PHB (poly-3-hydroxybutyrate) biosynthesis and phosphate/phosphonate transporters. However, different transcription profiles between bacteroids from two legumes were also uncovered for genes involved in the biosynthesis of exopolysaccharides, lipopolysaccharides, T3SS (type three secretion system) and effector proteins, cytochrome bd ubiquinol oxidase, PQQ (pyrroloquinoline quinone), cytochrome c550, pseudoazurin, biotin, phasins and glycolate oxidase, and in the metabolism of glutamate and phenylalanine.
Based on these transcriptomic results,19deletion mutants were constructed for corresponding differentially expressed genes. Nine mutants showed defects in bacteroids persistance in V. unguiculata nodules and these genes encode Phasin1, Phasin2, ATP-dependent carboxylate-amine ligase, Hypothetical protein, PRC-barrel domain protein, UspA, cytochrome bd-Ⅱ, and RibH respectively. Among these nine mutants, five and four mutants were impaired in infecting nodules of Cajanus cajan and Lablab purpureus, respectively; one mutant showed defects in bacteroids persistence in L. purpureus nodules. However no significant differences were observed between wild type strain and18/19mutants when they were inoculated on L. leucocephala. Thus we hypothesized that, in contrast to V. unguiculata, C. cajan and L. purpureus, L. leucocephala might provide rhizobia with more carbon and energy sources that could support normal symbiotic process when the above mentioned mutants were inoculated. Among these four lemume hosts, L. leucocephala and C. cajan formed indeterminate nodules whereas V. unguiculata and L. purpureus formed determinate nodules. Taken together, these findings suggest that the symbiotic role of the same gene of NGR234showed noticeable variations, when forming symbiosis with different legume hosts, in terms of the essentialbility for different symbiotic stages (infection or bacteroids differentiation). And these symbiotic phenotypes have no correlation with nodule types (indeterminate or determinate nodules).
All strains closely clustered with NGR234in the genome based phylogenetic tree can form nitrogen-fixing nodules with Glycine max/Glycine sojae, whereas NGR234can not. By constructing and screening a Tn5mutant library of NGR234, seven mutants were found to be able to form nitrogen-fixing nodules on G. sojae (1-1.6nodules per plant), though10%-30%of plants inoculated with these seven mutants did not have effective nodules. These results imply that multiple mutation events or some foreign genes might be needed by NGR234for establishing more stable and effective symbiosis with G. sojae. Interestingly, in this mutant library, a mutant of the gene encoding a LysR regulator formed effective nodules on C. cajan, L. leucocephala and V. unguiculata, but was impaired in infecting its primary host L. purpureus. Most homologs of this LysR regulator were present in pathogenic bacteria, indicating that NGR234could use certain mechanism similar to those pathogens to infect L. purpureus and that the coding gene of this regulator could have been laterally transferred to NGR234.
引文
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