{"title":"以尿素为基础的生物土壤结壳中氮的相互转移","authors":"Ana Mercedes Heredia-Velásquez, Soumyadev Sarkar, Finlay Warsop Thomas, Ariadna Cairó Baza, Ferran Garcia-Pichel","doi":"10.1093/ismejo/wrae246","DOIUrl":null,"url":null,"abstract":"Foundational to establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its “cyanosphere”. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus. vaginatus is likely central.","PeriodicalId":516554,"journal":{"name":"The ISME Journal","volume":"8 1","pages":""},"PeriodicalIF":0.0000,"publicationDate":"2024-12-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Urea-based mutualistic transfer of nitrogen in biological soil crusts\",\"authors\":\"Ana Mercedes Heredia-Velásquez, Soumyadev Sarkar, Finlay Warsop Thomas, Ariadna Cairó Baza, Ferran Garcia-Pichel\",\"doi\":\"10.1093/ismejo/wrae246\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"Foundational to establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its “cyanosphere”. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus. vaginatus is likely central.\",\"PeriodicalId\":516554,\"journal\":{\"name\":\"The ISME Journal\",\"volume\":\"8 1\",\"pages\":\"\"},\"PeriodicalIF\":0.0000,\"publicationDate\":\"2024-12-14\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"The ISME Journal\",\"FirstCategoryId\":\"1085\",\"ListUrlMain\":\"https://doi.org/10.1093/ismejo/wrae246\",\"RegionNum\":0,\"RegionCategory\":null,\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"\",\"JCRName\":\"\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"The ISME Journal","FirstCategoryId":"1085","ListUrlMain":"https://doi.org/10.1093/ismejo/wrae246","RegionNum":0,"RegionCategory":null,"ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"","JCRName":"","Score":null,"Total":0}
引用次数: 0
摘要
生物簇建立和恢复的基础是先驱蓝藻(包括广泛分布的微oleus vaginatus)与其 "蓝藻圈 "中的异养重氮生物之间以碳换氮的互助交换。在其他此类互生关系中,氮是以氨基酸或铵盐的形式转移的,通过特化结构、细胞附着或细胞内性来防止氮的损失。然而,在生物簇共生中,通过趋化作用实现的相对接近可以优化交换。我们推测,进一步的伙伴特异性可能来自于使用一种不寻常的氮载体--尿素。我们发现,具有代表性的互生菌 M. vaginatus PCC 9802 拥有尿素吸收基因、两个尿素分解系统基因和尿素循环基因,在与互生菌 Massilia sp.反过来,在共培养时,它过度表达尿素生物合成,但既不表达尿素酶,也不表达尿素吸收。在无氮培养基上,三种蓝藻分离物在与 M. vaginatus 共培养时释放尿素,而在单培养时则不释放尿素。相反,M. vaginatus PCC 9802 在低至微摩尔范围的尿素中生长。在自然生物群落中,尿素的浓度较低且稳定,无法支持大多数局部细菌的生长,但互生藻的聚集体构成了动态的微尺度尿素热点,蓝藻对尿素产生化学反应。协调的基因共调、培养的互生菌的生理学、自然界中尿素池的分布以及本地微生物种群的反应都表明,低浓度尿素可能是种间氮转移的主要载体,有助于实现伙伴特异性,而微囊藻罕见的高亲和性尿素/尿素系统可能是这种特异性的核心。
Urea-based mutualistic transfer of nitrogen in biological soil crusts
Foundational to establishment and recovery of biocrusts is a mutualistic exchange of carbon for nitrogen between pioneer cyanobacteria, including the widespread Microcoleus vaginatus, and heterotrophic diazotrophs in its “cyanosphere”. In other such mutualisms, nitrogen is transferred as amino acids or ammonium, preventing losses through specialized structures, cell apposition or intracellularity. Yet, in the biocrust symbiosis relative proximity achieved through chemotaxis optimizes the exchange. We posited that further partner specificity may stem from using an unusual nitrogen vehicle, urea. We show that representative mutualist M. vaginatus PCC 9802 possesses genes for urea uptake, two ureolytic systems, and the urea cycle, overexpressing only uptake and the rare urea carboxylase/allophanate hydrolase (uc/ah) when in co-culture with mutualist Massilia sp. METH4. In turn, it overexpresses urea biosynthesis, but neither urease nor urea uptake when in co-culture. On nitrogen-free medium, three cyanosphere isolates release urea in co-culture with M. vaginatus but not in monoculture. Conversely, M. vaginatus PCC 9802 grows on urea down to the low micromolar range. In natural biocrusts, urea is at low and stable concentrations that do not support the growth of most local bacteria, but aggregates of mutualists constitute dynamic microscale urea hotspots, and the cyanobacterium responds chemotactically to urea. The coordinated gene co-regulation, physiology of cultured mutualists, distribution of urea pools in nature, and responses of native microbial populations, all suggest that low-concentration urea is likely the main vehicle for interspecies N transfer, helping attain partner specificity, for which the rare high-affinity uc/ah system of Microcoleus. vaginatus is likely central.