Exploratory Growth in Streptomyces venezuelae Involves a Unique Transcriptional Program, Enhanced Oxidative Stress Response, and Profound Acceleration in Response to Glycerol
Exploratory Growth in Streptomyces venezuelae Involves a Unique Transcriptional Program, Enhanced Oxidative Stress Response, and Profound Acceleration in Response to Glycerol
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DOI：
10.1128/jb.00623-21
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发表时间：
2021-12
影响因子：
3.2
通讯作者：
Evan M F Shepherdson;Tina Netzker;Y. Stoyanov;M. Elliot
中科院分区：
文献类型：
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作者：
Evan M F Shepherdson;Tina Netzker;Y. Stoyanov;M. Elliot
探索是链霉菌的另一种生长策略，是对其他微生物或特定环境条件的响应。在这里，我们表明进入探索涉及全面的转录重编程，重点是初级代谢和调节/信号功能的变化。探索是最近发现的一些链霉菌的生长和行为模式，不同于它们经典的孢子生命周期。虽然关于探索性生长的初始环境条件和表型结果已经发现了很多，但这一过程如何在遗传水平上协调仍不清楚。我们使用RNA测序来调查模式生物委内瑞拉链霉菌在探索培养物的转录谱随时间的全球变化。转录组学分析揭示了影响多种细胞功能的基因表达的广泛变化。对差异表达调控元件的研究揭示了受影响的特定调控因子组，包括几种胞浆外功能（ECF） sigma因子的表达、第二信使信号通路和whb样转录因子（wbl）家族成员。主要代谢途径，特别是呼吸相关基因和氧化应激反应发生了显著变化；酶分析证实，与传统培养相比，探索培养表现出增强的氧化应激反应。委内瑞拉螺中甘油分解代谢基因表达的变化导致发现，在生长培养基中补充甘油促进了探索的急剧加速。这种效果似乎是甘油作为替代碳源所特有的，并且这种反应在其他具有勘探能力的物种中广泛保守。探索是链霉菌的另一种生长策略，是对其他微生物或特定环境条件的响应。在这里，我们表明进入探索涉及全面的转录重编程，重点是初级代谢和调节/信号功能的变化。有趣的是，许多转录因子类别在进入探索时被下调。相反，呼吸相关基因被强烈诱导，这伴随着氧化应激反应的增强。值得注意的是，我们的转录分析表明甘油可能在探索中发挥作用，我们发现补充甘油显著增强了许多链菌的探索反应。这项工作揭示了新的调控和代谢线索，影响一个迷人的新的微生物行为。
Exploration represents an alternative growth strategy for Streptomyces bacteria and is initiated in response to other microbes or specific environmental conditions. Here, we show that entry into exploration involves comprehensive transcriptional reprogramming, with an emphasis on changes in primary metabolism and regulatory/signaling functions. ABSTRACT Exploration is a recently discovered mode of growth and behavior exhibited by some Streptomyces species that is distinct from their classical sporulating life cycle. While much has been uncovered regarding initiating environmental conditions and phenotypic outcomes of exploratory growth, how this process is coordinated at a genetic level remains unclear. We used RNA sequencing to survey global changes in the transcriptional profile of exploring cultures over time in the model organism Streptomyces venezuelae. Transcriptomic analyses revealed widespread changes in gene expression impacting diverse cellular functions. Investigations into differentially expressed regulatory elements revealed specific groups of regulatory factors to be impacted, including the expression of several extracytoplasmic function (ECF) sigma factors, second messenger signaling pathways, and members of the whiB-like (wbl) family of transcription factors. Dramatic changes were observed among primary metabolic pathways, especially among respiration-associated genes and the oxidative stress response; enzyme assays confirmed that exploring cultures exhibit an enhanced oxidative stress response compared with classically growing cultures. Changes in the expression of the glycerol catabolic genes in S. venezuelae led to the discovery that glycerol supplementation of the growth medium promotes a dramatic acceleration of exploration. This effect appears to be unique to glycerol as an alternative carbon source, and this response is broadly conserved across other exploration-competent species. IMPORTANCE Exploration represents an alternative growth strategy for Streptomyces bacteria and is initiated in response to other microbes or specific environmental conditions. Here, we show that entry into exploration involves comprehensive transcriptional reprogramming, with an emphasis on changes in primary metabolism and regulatory/signaling functions. Intriguingly, a number of transcription factor classes were downregulated upon entry into exploration. In contrast, respiration-associated genes were strongly induced, and this was accompanied by an enhanced oxidative stress response. Notably, our transcriptional analyses suggested that glycerol may play a role in exploration, and we found that glycerol supplementation dramatically enhanced the exploration response in many streptomycetes. This work sheds new light on the regulatory and metabolic cues that influence a fascinating new microbial behavior.