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.

中文翻译：

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生物土壤结皮中基于尿素的氮共生转移


生物结皮建立和恢复的基础是先锋蓝细菌（包括广泛分布的 Microcoleus vaginatus）和其“蓝层”中的异养重氮营养生物之间的碳与氮的相互交换。在其他此类共生关系中，氮以氨基酸或铵态的形式转移，防止通过特殊结构、细胞并置或细胞内性进行损失。然而，在生物壳共生中，通过趋化性实现的相对接近优化了交换。我们假设进一步的伴侣特异性可能源于使用一种不寻常的氮载体尿素。我们表明，代表性共生者 M. vaginatus PCC 9802 具有尿素摄取、两个尿道溶解系统和尿素循环的基因，在与共生者 Massilia sp. METH4 共培养时，仅过表达摄取和罕见的尿素羧化酶/异体水解酶 （uc/ah）。反过来，它过表达尿素生物合成，但在共培养时既不表达脲酶也不摄取尿素。在无氮培养基上，三种氰球分离株在与 M. vaginatus 共培养中释素，但在单一培养中不释素。相反，M. vaginatus PCC 9802 在尿素上生长到低微摩尔范围。在天然生物结皮中，尿素处于低且稳定的浓度，不支持大多数局部细菌的生长，但共生菌的聚集体构成了动态的微尺度尿素热点，蓝细菌对尿素有趋化反应。协调的基因共调控、培养互惠生物的生理学、自然界中尿素池的分布以及天然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，有助于获得伴侣特异性，为此，Microcoleus 罕见的高亲和力 uc/ah 系统。 阴道可能位于中央。