"Ca. Nitrosocosmicus" members are the dominant archaea associated with plant rhizospheres.

IF 3.7 2区 生物学 Q2 MICROBIOLOGY mSphere Pub Date : 2024-11-12 DOI:10.1128/msphere.00821-24
Ui-Ju Lee, Joo-Han Gwak, Seungyeon Choi, Man-Young Jung, Tae Kwon Lee, Hojin Ryu, Samuel Imisi Awala, Wolfgang Wanek, Michael Wagner, Zhe-Xue Quan, Sung-Keun Rhee
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Abstract

Archaea catalyzing the first step of nitrification in the rhizosphere possibly have an influence on plant growth and development. In this study, we found a distinct archaeal community, dominated by ammonia-oxidizing archaea (AOA), associated with the root system of pepper (Capsicum anuum L.) and ginseng plants (Panax ginseng C.A. Mey.) compared to bulk soil not penetrated by roots. While the abundance of total AOA decreased in the rhizosphere soils, AOA related to "Candidatus Nitrosocosmicus," which harbor gene encoding manganese catalase (MnKat) in contrast to most other AOA, dominated the AOA community in the rhizosphere soils. For both plant species, the ratio of copy numbers of the AOA MnKat gene to the amoA gene (encoding the ammonia monooxygenase subunit A) was significantly higher in the rhizospheres than in bulk soils. In contrast to MnKat-negative strains from other AOA clades, the catalase activity of a representative isolate of "Ca. Nitrosocosmicus" was demonstrated. Members of this clade were enriched in H2O2-amended bulk soils, and constitutive expression of their MnKat gene was observed in both bulk and rhizosphere soils. Due to their abundance, "Ca. Nitrosocosmicus" members can be considered important players mediating the nitrification process in rhizospheres. The dominance of this MnKat-containing AOA in rhizospheres of agriculturally important plants hints at a previously overlooked AOA-plant interaction.

Importance: Ammonia-oxidizing archaea (AOA) are widespread in terrestrial environments and outnumber other ammonia oxidizers in the rhizosphere, possibly exerting an influence on plant growth and development. However, little is known about the selection forces that shape their composition, functions, survival, and proliferation strategies in the rhizosphere. Here, we observed a distinct AOA community on root systems of two different plant species compared to bulk soil. Our results show that the "Ca. Nitrosocosmicus" clade, which possesses functional MnKat genes unlike most other AOA, dominated the rhizosphere soils. Moreover, members of this clade were enriched in H2O2-amended bulk soil, which mimics the ROS stress in root systems. While research on AOA-plant interactions in the rhizosphere is still in its infancy, these findings suggest that "Ca. Nitrosocosmicus" may be an important clade of AOA with potential AOA-plant interaction.

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"Ca.Nitrosocosmicus "成员是与植物根瘤相关的主要古菌。
催化根圈硝化第一步的古细菌可能会对植物的生长和发育产生影响。在这项研究中,我们发现辣椒(Capsicum anuum L.)和人参(Panax ginseng C.A. Mey.虽然根圈土壤中总 AOA 的丰度有所下降,但与大多数其他 AOA 不同,根圈土壤中的 AOA 群落主要由与 "Candidatus Nitrosocosmicus "相关的 AOA 组成,该 AOA 含有编码锰过氧化氢酶(MnKat)的基因。对于这两种植物来说,根瘤菌圈中 AOA MnKat 基因与 amoA 基因(编码氨单氧合酶亚基 A)的拷贝数之比明显高于大体积土壤。与其他 AOA 支系中 MnKat 阴性的菌株相比,"Ca. Nitrosocosmicus "的一个代表性分离株的过氧化氢酶活性较高。Nitrosocosmicus "的过氧化氢酶活性得到了证实。该支系的成员富集于经 H2O2-修饰的块状土壤中,在块状土壤和根瘤土壤中都观察到其 MnKat 基因的组成型表达。由于 "Ca.Nitrosocosmicus "成员可被视为根瘤菌圈硝化过程的重要介导者。这种含 MnKat 的 AOA 在具有重要农业价值的植物根瘤菌圈中占主导地位,暗示了一种以前被忽视的 AOA 与植物之间的相互作用:氨氧化古细菌(AOA)广泛存在于陆地环境中,在根瘤菌圈中数量超过其他氨氧化菌,可能对植物的生长和发育产生影响。然而,人们对其在根瘤菌层中的组成、功能、生存和增殖策略的选择力知之甚少。在这里,我们观察到两种不同植物根系上的 AOA 群落与土壤中的 AOA 群落截然不同。结果表明,"Ca.Nitrosocosmicus "支系与大多数其他 AOA 不同,它拥有功能性 MnKat 基因,在根圈土壤中占主导地位。此外,该支系的成员在经 H2O2-修饰的块状土壤中富集,这种土壤模拟了根系中的 ROS 压力。虽然对根圈中 AOA 与植物相互作用的研究仍处于起步阶段,但这些发现表明,"Ca.Nitrosocosmicus "可能是AOA的一个重要支系,具有潜在的AOA-植物相互作用。
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来源期刊
mSphere
mSphere Immunology and Microbiology-Microbiology
CiteScore
8.50
自引率
2.10%
发文量
192
审稿时长
11 weeks
期刊介绍: mSphere™ is a multi-disciplinary open-access journal that will focus on rapid publication of fundamental contributions to our understanding of microbiology. Its scope will reflect the immense range of fields within the microbial sciences, creating new opportunities for researchers to share findings that are transforming our understanding of human health and disease, ecosystems, neuroscience, agriculture, energy production, climate change, evolution, biogeochemical cycling, and food and drug production. Submissions will be encouraged of all high-quality work that makes fundamental contributions to our understanding of microbiology. mSphere™ will provide streamlined decisions, while carrying on ASM''s tradition for rigorous peer review.
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