Myxococcus xanthus fruiting body morphology is important for spore recovery after exposure to environmental stress.

IF 3.9 2区 生物学 Q2 BIOTECHNOLOGY & APPLIED MICROBIOLOGY Applied and Environmental Microbiology Pub Date : 2024-10-23 Epub Date: 2024-10-04 DOI:10.1128/aem.01660-24
Dave Lall, Maike M Glaser, Penelope I Higgs
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Abstract

Environmental microorganisms have evolved a variety of strategies to survive fluctuations in environmental conditions, including the production of biofilms and differentiation into spores. Myxococcus xanthus are ubiquitous soil bacteria that produce starvation-induced multicellular fruiting bodies filled with environmentally resistant spores (a specialized biofilm). Isolated spores have been shown to be more resistant than vegetative cells to heat, ultraviolet radiation, and desiccation. The evolutionary advantage of producing spores inside fruiting bodies is not clear. Here, we examine a hypothesis that the fruiting body provides additional protection from environmental insults. We developed a high-throughput method to compare the recovery (outgrowth) of distinct cell types (vegetative cells, free spores, and spores within intact fruiting bodies) after exposure to ultraviolet radiation or desiccation. Our data indicate that haystack-shaped fruiting bodies protect spores from extended UV radiation but do not provide additional protection from desiccation. Perturbation of fruiting body morphology strongly impedes recovery from both UV exposure and desiccation. These results hint that the distinctive fruiting bodies produced by different myxobacterial species may have evolved to optimize their persistence in distinct ecological niches.IMPORTANCEEnvironmental microorganisms play an important role in the production of greenhouse gases that contribute to changing climate conditions. It is imperative to understand how changing climate conditions feedback to influence environmental microbial communities. The myxobacteria are environmentally ubiquitous social bacteria that influence the local microbial community composition. Defining how these bacteria are affected by environmental insults is a necessary component of predicting climatic feedback effects. When starved, myxobacteria produce multicellular fruiting bodies filled with spores. As spores are resistant to a variety of environmental insults, the evolutionary advantage of building a fruiting body is not clear. Using the model myxobacterium, Myxococcus xanthus, we demonstrate that the tall, haystack-shaped fruiting body morphology enables significantly more resistance to UV exposure than the free spores. In contrast, fruiting bodies are slightly detrimental to recovery from extended desiccation, an effect that is strongly exaggerated if fruiting body morphology is perturbed. These results suggest that the variety of fruiting body morphologies observed in the myxobacteria may dictate their relative resistance to changing climate conditions.

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黄曲霉菌子实体形态对暴露于环境压力后的孢子恢复非常重要。
环境微生物进化出了多种策略来应对环境条件的波动,包括生成生物膜和分化成孢子。黄曲霉菌是一种无处不在的土壤细菌,会在饥饿状态下产生多细胞子实体,子实体中充满了耐环境的孢子(一种特殊的生物膜)。研究表明,分离的孢子比无性细胞更耐高温、紫外线辐射和干燥。在子实体内产生孢子的进化优势尚不清楚。在此,我们研究了一个假设,即子实体可提供额外的保护,使孢子免受环境侵害。我们开发了一种高通量方法来比较不同细胞类型(无性细胞、游离孢子和完整子实体内的孢子)在暴露于紫外线辐射或干燥后的恢复(生长)情况。我们的数据表明,干草堆状子实体能保护孢子免受长时间的紫外线辐射,但不能提供额外的干燥保护。干扰子实体形态会严重阻碍孢子从紫外线照射和干燥中恢复。这些结果表明,不同种类的霉菌所产生的独特子实体可能是为了优化其在不同生态位中的持久性而进化而来的。当务之急是了解不断变化的气候条件如何反馈影响环境微生物群落。粘菌是环境中无处不在的社会性细菌,它们会影响当地微生物群落的组成。确定这些细菌如何受到环境污染的影响是预测气候反馈效应的必要组成部分。当饥饿时,粘菌会产生充满孢子的多细胞子实体。由于孢子可抵抗各种环境侵袭,建立子实体的进化优势尚不明确。我们利用黄腐霉菌(Myxococcus xanthus)这一模式霉菌证明,高大、干草堆状的子实体形态比游离孢子更能抵抗紫外线照射。相反,子实体对长时间干燥后的恢复略有不利,如果扰乱子实体形态,这种影响会被大大夸大。这些结果表明,在霉菌中观察到的各种子实体形态可能决定了它们对不断变化的气候条件的相对抵抗力。
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来源期刊
Applied and Environmental Microbiology
Applied and Environmental Microbiology 生物-生物工程与应用微生物
CiteScore
7.70
自引率
2.30%
发文量
730
审稿时长
1.9 months
期刊介绍: Applied and Environmental Microbiology (AEM) publishes papers that make significant contributions to (a) applied microbiology, including biotechnology, protein engineering, bioremediation, and food microbiology, (b) microbial ecology, including environmental, organismic, and genomic microbiology, and (c) interdisciplinary microbiology, including invertebrate microbiology, plant microbiology, aquatic microbiology, and geomicrobiology.
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