Metagenomic insights into inhibition of soil microbial carbon metabolism by phosphorus limitation during vegetation succession.

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-10-23 eCollection Date: 2024-01-01 DOI:10.1093/ismeco/ycae128
Haocai Wang, Hang Wang, Thomas W Crowther, Kazuo Isobe, Peter B Reich, Ryunosuke Tateno, Weiyu Shi
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Abstract

There is growing awareness of the need for regenerative practices in the fight against biodiversity loss and climate change. Yet, we lack a mechanistic understanding of how microbial community composition and functioning are likely to change alongside transition from high-density tillage to large-scale vegetation restoration. Here, we investigated the functional dynamics of microbial communities following a complete vegetation successional chronosequence in a subtropical zone, Southwestern China, using shotgun metagenomics approaches. The contents of total soil phosphorus (P), available P, litter P, and microbial biomass P decreased significantly during vegetation succession, indicating that P is the most critical limiting nutrient. The abundance of genes related to P-uptake and transport, inorganic P-solubilization, organic P-mineralization, and P-starvation response regulation significantly increased with successional time, indicating an increased microbial "mining" for P under P limitation. Multi-analysis demonstrated microbial P limitation strongly inhibits carbon (C) catabolism potential, resulting in a significant decrease in carbohydrate-active enzyme family gene abundances. Nevertheless, over successional time, microorganisms increased investment in genes involved in degradation-resistant compounds (lignin and its aromatic compounds) to acquire P resources in the litter. Our study provides functional gene-level insights into how P limitation during vegetation succession in subtropical regions inhibits soil microbial C metabolic processes, thereby advancing our understanding of belowground C cycling and microbial metabolic feedback during forest restoration.

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植被演替过程中磷限制对土壤微生物碳代谢抑制的元基因组学启示。
人们越来越意识到,在应对生物多样性丧失和气候变化的过程中,需要采用再生方法。然而,我们对微生物群落的组成和功能如何可能随着从高密度耕作到大规模植被恢复的过渡而发生变化缺乏机制上的了解。在此,我们采用霰弹枪元基因组学方法研究了中国西南亚热带地区完整植被演替时序后微生物群落的功能动态。在植被演替过程中,土壤总磷、可利用磷、枯落物磷和微生物生物量磷的含量显著下降,表明磷是最关键的限制性养分。与磷吸收和转运、无机磷溶解、有机磷矿化和磷饥饿反应调节相关的基因丰度随着演替时间的延长而显著增加,表明在磷限制条件下微生物对磷的 "挖掘 "增加。多重分析表明,微生物的 P 限制强烈抑制了碳(C)分解潜力,导致碳水化合物活性酶家族基因丰度显著下降。然而,随着演替时间的推移,微生物增加了对涉及抗降解化合物(木质素及其芳香族化合物)基因的投资,以获取枯落物中的钾资源。我们的研究从功能基因水平上揭示了亚热带地区植被演替过程中P限制是如何抑制土壤微生物C代谢过程的,从而加深了我们对森林恢复过程中地下C循环和微生物代谢反馈的理解。
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