Heredia-Velásquez Ana Mercedes, Sarkar Soumyadev, Thomas Finlay Warsop, Baza Ariadna Cairó, Garcia-Pichel Ferran
Center for Fundamental and Applied Microbiomics, Biodesign Institute, Arizona State University, Tempe, AZ 85287, United States.
School of Life Sciences, Arizona State University, Tempe, AZ 85287, United States.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wrae246.
Foundational to the 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.
生物结皮的建立和恢复的基础是先锋蓝细菌（包括广泛分布的鞘丝藻）与其“蓝细菌圈”中的异养固氮菌之间碳与氮的互利交换。在其他此类共生关系中，氮以氨基酸或铵的形式转移，通过特殊结构、细胞并列或细胞内作用防止损失。然而，在生物结皮共生关系中，通过趋化作用实现的相对接近优化了这种交换。我们推测，进一步的伙伴特异性可能源于使用一种不寻常的氮载体——尿素。我们发现，代表性的共生菌鞘丝藻PCC 9802拥有尿素摄取基因、两个尿素分解系统和尿素循环，当与共生菌马赛菌属METH4共培养时，仅过表达摄取和罕见的尿素羧化酶/脲基甲酸水解酶（uc/ah）。反过来，当共培养时，它过表达尿素生物合成，但不过表达脲酶或尿素摄取。在无氮培养基上，三种蓝细菌圈分离物与鞘丝藻共培养时会释放尿素，但单独培养时不会。相反，鞘丝藻PCC 9802能在低至低微摩尔浓度的尿素上生长。在天然生物结皮中，尿素浓度低且稳定，不支持大多数当地细菌生长，但共生菌聚集体构成动态的微观尿素热点，蓝细菌对尿素有趋化反应。协调的基因共调控、培养共生菌的生理学、自然界中尿素库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，鞘丝藻罕见的高亲和力uc/ah系统可能在其中起核心作用。
