Divergence and convergence in epiphytic and endophytic phyllosphere bacterial communities of rice landraces.

IF 3.7 2区 生物学 Q2 MICROBIOLOGY
mSphere Pub Date : 2024-10-30 DOI:10.1128/msphere.00765-24
Pratibha Sanjenbam, Deepa Agashe
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引用次数: 0

Abstract

Phyllosphere-associated microbes can significantly alter host plant fitness, with distinct functions provided by bacteria inhabiting the epiphytic (external surface) vs endophytic niches (internal leaf tissue). Hence, it is important to understand the assembly and stability of these phyllosphere communities, especially in field conditions. Broadly, epiphytic communities should encounter more environmental fluctuations and frequent immigration, whereas endophytic microbiota should face stronger host selection. As a result, we expect greater variability in epiphytic than endophytic communities. We analyzed the structure and stability of leaf phyllosphere microbiota of four traditionally cultivated rice landraces and one commercial variety from northeast India grown in the field for 3 consecutive years, supplemented with opportunistic sampling of eight other landraces. Epiphytic and endophytic bacterial communities shared dominant core genera such as Methylobacterium and Sphingomonas. Consistent with an overall strong environmental effect, both communities varied more across sampling years than across host landraces. Seeds sampled from a focal landrace did not support vertical transmission of phyllosphere bacteria, suggesting that both types of communities are assembled anew each generation. Despite these points of convergence, epiphytic communities had distinct composition and significantly higher microbial load and were more rich, diverse, modular, and unstable than endophytic communities. Finally, focused sampling of one landrace across developmental stages showed that the divergence between the two types of communities arose primarily at the flowering stage. Thus, our results show both convergent and divergent patterns of community assembly and composition in distinct phyllosphere niches in rice, identifying key bacterial genera and host developmental stages that may aid agricultural interventions to increase rice yield.IMPORTANCEPhyllosphere (leaf-associated) microbes significantly impact plant fitness, making it crucial to understand how these communities are assembled and maintained. While many studies have analyzed epiphytic (surface) phyllosphere communities, we have a relatively poor understanding of endophytic communities which colonize the very distinct niche formed inside leaf tissues. We found that across several rice landraces, both communities are largely colonized by the same core genera, indicating divergence at the species level across the two leaf niches and highlighting the need to understand the mechanisms underlying this divergence. Surprisingly, both epiphytic and endophytic communities were only weakly shaped by the host landrace, with a much greater role for environmental factors that likely vary over time. Thus, microbiome-based agricultural interventions for increasing productivity could perhaps be generalized across rice varieties but would need to account for the temporal instability of the microbiota. Our results thus highlight the importance of data sets such as ours-with extensive sampling across landraces and years-for understanding phyllosphere microbiota and their applications in the field.

水稻陆稻附生和内生叶球细菌群落的分化与趋同。
叶球相关微生物可显著改变寄主植物的适应性,栖息在附生(外部表面)和内生(内部叶片组织)壁龛中的细菌具有不同的功能。因此,了解这些叶球群落的组成和稳定性非常重要,尤其是在田间条件下。一般来说,附生群落会遇到更多的环境波动和频繁的移民,而内生微生物群落则会面临更强的宿主选择。因此,我们预计附生生物群落的变异性要大于内生生物群落。我们分析了印度东北部连续 3 年在田间种植的 4 个传统栽培水稻陆稻品种和 1 个商业品种的叶肉微生物群的结构和稳定性,并对其他 8 个陆稻品种进行了机会性采样。附生细菌群落和内生细菌群落共享优势核心菌属,如 Methylobacterium 和 Sphingomonas。这两种群落在不同采样年份的差异比不同寄主品种的差异更大,这与整体环境的强烈影响是一致的。从一个重点陆生品系采样的种子不支持叶球细菌的垂直传播,这表明这两种群落每一代都是重新组合的。尽管存在这些趋同点,但附生群落具有独特的组成,微生物负载量明显高于内生群落,并且更加丰富、多样、模块化和不稳定。最后,对一个陆生品种不同发育阶段的集中取样表明,两种群落之间的差异主要出现在开花阶段。因此,我们的研究结果显示了水稻不同叶球壁龛中群落组装和组成的趋同和分化模式,确定了关键的细菌属和宿主发育阶段,这可能有助于农业干预措施以提高水稻产量。虽然许多研究分析了附生(表面)叶球群落,但我们对定植于叶片组织内部形成的非常独特的生态位的内生群落的了解相对较少。我们发现,在几个水稻品种中,这两种群落主要由相同的核心种属定殖,这表明两种叶片壁龛在物种水平上存在差异,并强调了了解这种差异背后机制的必要性。令人惊讶的是,附生和内生生物群落受宿主品种的影响都很微弱,环境因素的作用要大得多,而环境因素很可能随时间而变化。因此,基于微生物群的农业干预措施或许可以在不同水稻品种间推广,但需要考虑微生物群的时间不稳定性。因此,我们的研究结果凸显了像我们这样的数据集--跨品种、跨年份的广泛采样--对于了解叶球微生物群及其在田间应用的重要性。
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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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