Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere

Spatial segregation of the biological soil crust microbiome around its foundational cyanobacterium, Microcoleus vaginatus, and the formation of a nitrogen-fixing cyanosphere
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DOI:
10.1186/s40168-019-0661-2
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发表时间:
2019-04-03
期刊:
影响因子:
15.5
通讯作者:
Garcia-Pichel, Ferran
Garcia-Pichel, Ferran
中科院分区:
生物学1区
文献类型:
--
作者:
Couradeau, Estelle;Giraldo-Silva, Ana;Garcia-Pichel, Ferran

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背景:形成束的丝状非固氮蓝藻阴道微鞘藻是先驱的初级生产者,通常是生物结皮微生物组的主要成员,也是泄漏有机碳的主要来源。我们假设,通过类比植物根的根际,M. vaginatus 可能会塑造其周围的异养微生物种群,形成专门的蓝藻圈。结果:我们发现一小部分选定的 OTU 子集在靠近 M. vaginatus 的地方显着富集。此外,我们还发现,大多数细菌(相当于大约三分之二的读数)远离这种蓝细菌时显着更加丰富。系统发育位置表明,蓝藻圈的所有典型成员都是富营养生物,并且许多是固氮生物(附加文件 1:表 S2 和 S3)。事实上,根据 qPCR 评估,蓝圈中的固氮基因比大量生物结皮土壤中的固氮基因丰富几个数量级。相反,对光、二氧化碳和低有机碳浓度的竞争至少定义了一部分与蓝藻分离的 OTU。结论:我们表明 M. vaginatus 是生物结皮微生物组的重要空间组织者。一方面,它具有成分差异化的蓝藻圈,集中了固氮功能。我们认为,基于 M. vaginatus 和富营养型固氮菌之间的碳换氮交换的互利共生有助于维持这种蓝藻圈,并且该群落构成了真正的先锋群落,能够在贫氮土壤上进行殖民化。另一方面,大量的生物结皮群落成员可能通过对光或二氧化碳的竞争,或者因为对寡营养的偏好而远离 M. vaginatus 附近。
Background: The bundle-forming, filamentous, non-nitrogen-fixing cyanobacterium Microcoleus vaginatus is a pioneer primary producer, often the dominant member of the biocrust microbiome, and the main source of leaked organic carbon. We hypothesized that, by analogy to the rhizosphere of plant roots, M. vaginatus may shape the microbial populations of heterotrophs around it, forming a specialized cyanosphere.Results: We found that a small, selected subset of OTUs was significantly enriched in close proximity to M. vaginatus. Furthermore, we also found that a majority of bacteria (corresponding to some two thirds of the reads) were significantly more abundant away from this cyanobacterium. Phylogenetic placements suggest that all typical members of the cyanosphere were copiotrophs and that many were diazotrophs (Additional file 1: Tables S2 and S3). Nitrogen fixation genes were in fact orders of magnitude more abundant in this cyanosphere than in the bulk biocrust soil as assessed by qPCR. By contrary, competition for light, CO2, and low organic carbon concentrations defined at least a part of the OTUs segregating from the cyanobacterium.Conclusions: We showed that M. vaginatus acts as a significant spatial organizer of the biocrust microbiome. On the one hand, it possesses a compositionally differentiated cyanosphere that concentrates the nitrogen-fixing function. We propose that a mutualism based on C for N exchange between M. vaginatus and copiotrophic diazotrophs helps sustains this cyanosphere and that this consortium constitutes the true pioneer community enabling the colonization of nitrogen-poor soils. On the other hand, a large number of biocrust community members segregate away from the vicinity of M. vaginatus, potentially through competition for light or CO2 , or because of a preference for oligotrophy.