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对螺旋蛋白B生产的过度投资限制了宿主内的生长,并有利于螺旋体昆虫内共生体的垂直传播


来源: Florent Masson et al  发布日期: 2022-08-31  访问量: 113


昆虫经常有内共生体,即寄主组织中的细菌。通过内共生体从寄主母亲到其后代的垂直传播,这些关联在进化时间尺度上稳定地维持。一些内共生生物操纵宿主繁殖以促进自然种群内的传播。因此,这种感染对昆虫的生理和进化有重大影响。然而,技术障碍限制了我们对昆虫-内共生体相互作用的分子机制的理解。在这里,我们使用易驯服的昆虫果蝇及其自然内共生体poulsonii螺旋体来研究内共生伙伴之间的营养相互作用。使用功能分析、代谢组学和蛋白质组学的组合,我们表明单个螺旋体膜凝集素螺旋蛋白B(SpiB)的丰度和氨基酸组成决定了内共生体的氨基酸需求,并决定了其在宿主组织内的增殖
标签: 螺旋蛋白B、共生体
 

Disproportionate investment in Spiralin B production limits in-host growth and favors the vertical transmission of Spiroplasma insect endosymbionts

Florent Masson3,1,Samuel Rommelaere1, Fanny Schüpfer1,Jean-Philippe Boquete1,Bruno Lemaitre 3

1Global Health Institute, School of Life Sciences, École Polytechnique Fédérale de Lausanne, Lausanne, 1015 Switzerland
2Present address: School of Biological Sciences, University of Bristol, Bristol, BS8 1TQ, United Kingdom.
 
Significance
Most insects harbor bacterial endosymbionts within their tissues, which have major impacts on their physiology, ecology, and evolution. We investigate mechanisms that regulate such interaction between the fly Drosophila and its natural bacterial endosymbiont Spiroplasma poulsonii Melanogaster Sex-Ratio Organism (MSRO). MSRO grows in the fly hemolymph and is vertically transmitted across generations. We show that Spiralin B has major impacts on these two key features: while being involved in vertical transmission, its massive production monopolizes essential amino acids and impacts bacterial growth in nutrient-limited conditions. Our work illustrates that a single bacterial protein can couple key aspects of an endosymbiont lifestyle (its ability to proliferate in host tissues and to be vertically transmitted), thus maintaining the interaction over evolutionary timescales.
大多数昆虫的组织中都有细菌内共生体,这对它们的生理、生态和进化有重大影响。我们研究了调节果蝇与其天然细菌内共生体poulsonii黑腹螺旋体性比生物体(MSRO)之间相互作用的机制。MSRO在蝇血淋巴中生长,并跨代垂直传播。我们表明,螺旋蛋白B对这两个关键特征有重大影响:在参与垂直传播的同时,其大量生产垄断了必需氨基酸,并影响了营养有限条件下的细菌生长。我们的研究表明,单个细菌蛋白可以结合内共生体生活方式的关键方面(其在宿主组织中增殖和垂直传播的能力),从而在进化时间尺度上保持相互作用。

Abstract
Insects frequently harbor endosymbionts, which are bacteria housed within host tissues. These associations are stably maintained over evolutionary timescales through vertical transmission of endosymbionts from host mothers to their offspring. Some endosymbionts manipulate host reproduction to facilitate spread within natural populations. Consequently, such infections have major impacts on insect physiology and evolution. However, technical hurdles have limited our understanding of the molecular mechanisms underlying such insect–endosymbiont interactions. Here, we investigate the nutritional interactions between endosymbiotic partners using the tractable insect Drosophila melanogaster and its natural endosymbiont Spiroplasma poulsonii. Using a combination of functional assays, metabolomics, and proteomics, we show that the abundance and amino acid composition of a single Spiroplasma membrane lectin, Spiralin B (SpiB), dictates the amino acid requirements of the endosymbiont and determines its proliferation within host tissues. Ectopically increasing SpiB levels in host tissues disrupts localization of endosymbionts in the fly egg chambers and decreases vertical transmission. We find that SpiB is likely to be required by the endosymbiont to enter host oocytes, which may explain the massive investment of S. poulsonii in SpiB synthesis. SpiB both permits vertical transmission of the symbiont and limits its growth in nutrient-limiting conditions for the host; therefore, a single protein plays a pivotal role in ensuring durability of the interaction in a variable environment.
昆虫经常有内共生体,即寄主组织中的细菌。通过内共生体从寄主母亲到其后代的垂直传播,这些关联在进化时间尺度上稳定地维持。一些内共生生物操纵宿主繁殖以促进自然种群内的传播。因此,这种感染对昆虫的生理和进化有重大影响。然而,技术障碍限制了我们对昆虫-内共生体相互作用的分子机制的理解。在这里,我们使用易驯服的昆虫果蝇及其自然内共生体poulsonii螺旋体来研究内共生伙伴之间的营养相互作用。使用功能分析、代谢组学和蛋白质组学的组合,我们表明单个螺旋体膜凝集素螺旋蛋白B(SpiB)的丰度和氨基酸组成决定了内共生体的氨基酸需求,并决定了其在宿主组织内的增殖。体外增加宿主组织中的SpiB水平扰乱了内共生体在蝇卵室内的定位,并减少了垂直传播。我们发现,内共生体可能需要SpiB才能进入宿主卵母细胞,这可能解释了波尔索尼氏菌在SpiB合成方面的大量投资。SpiB既允许共生体的垂直传播,又限制其在宿主营养限制条件下的生长;因此,单个蛋白质在确保可变环境中相互作用的耐久性方面起着关键作用。

 


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