Garfias-Gallegos Diego, Pardo-De la Hoz Carlos J, Haughland Diane L, Magain Nicolas, Aguero Blanka, Miadlikowska Jolanta, Lutzoni François
Department of Biology, Duke University, Durham, NC 27708, United States.
Department of Renewable Resources, Faculty of Agricultural, Life & Environmental Sciences, University of Alberta, Edmonton, AB T6G 2H1, Canada.
ISME J. 2025 Jan 2;19(1). doi: 10.1093/ismejo/wraf166.
Nostoc cyanobacteria are among the few organisms capable of fixing both carbon and nitrogen. These metabolic features are essential for the cyanolichen symbiosis, where Nostoc supplies both carbon (as glucose) and nitrogen (as ammonium) to a cyanolichen-forming fungal partner. This nutrient flow was established by seminal biochemical studies published in the 20th century. Since then, cyanolichen metabolism has received little attention, and the molecular mechanisms that underlie the physiology of lichenized Nostoc remain mostly unknown. Here, we aimed to elucidate the genomic and transcriptional changes that enable Nostoc's metabolic role in cyanolichens. We used comparative genomics across 243 genomes of Nostoc s. lat. coupled with metatranscriptomic experiments using Peltigera cyanolichens. We found that genes for photoautotrophic carbon fixation are upregulated in lichenized Nostoc. This likely results in a higher rate of carbon fixation that allows Nostoc to provide carbon to the fungal partner while meeting its own metabolic needs. We also found that the transfer of ammonium from Nostoc to the lichen-forming fungus is facilitated by two molecular mechanisms: (i) transcriptional downregulation of glutamine synthetase, the key enzyme responsible for ammonium assimilation in Nostoc; and (ii) frequent losses of a putative high-affinity ammonium permease, which likely reduces Nostoc's capacity to recapture leaked ammonium. Finally, we found that the development of motile hormogonia is downregulated in lichenized Nostoc, which resembles the repression of motility in Nostoc symbionts after they colonize symbiotic cavities of their plant hosts. Our results pave the way for a revival of cyanolichen ecophysiology in the omics era.
念珠藻蓝细菌是少数能够同时固定碳和氮的生物之一。这些代谢特征对于蓝藻地衣共生至关重要，在这种共生关系中，念珠藻为形成蓝藻地衣的真菌伙伴提供碳（以葡萄糖形式）和氮（以铵形式）。这种养分流动是由20世纪发表的开创性生化研究确定的。从那时起，蓝藻地衣代谢很少受到关注，地衣化念珠藻生理学背后的分子机制仍然大多未知。在这里，我们旨在阐明使念珠藻在蓝藻地衣中发挥代谢作用的基因组和转录变化。我们对243个广义念珠藻基因组进行了比较基因组学研究，并结合使用蓝藻地卷进行了宏转录组实验。我们发现，地衣化念珠藻中光合自养碳固定相关基因上调。这可能导致更高的碳固定速率，使念珠藻能够在满足自身代谢需求的同时为真菌伙伴提供碳。我们还发现，铵从念珠藻转移到形成地衣的真菌有两种分子机制：（i）谷氨酰胺合成酶的转录下调——谷氨酰胺合成酶是念珠藻中负责铵同化的关键酶；（ii）一种假定的高亲和力铵通透酶频繁缺失，这可能会降低念珠藻重新捕获泄漏铵的能力。最后，我们发现地衣化念珠藻中运动型藻殖段的发育受到抑制，这类似于念珠藻共生体在定殖于植物宿主的共生腔后运动性受到的抑制。我们的研究结果为在组学时代复兴蓝藻地衣生态生理学铺平了道路。
