Aphid thermal tolerance is governed by a point mutation in bacterial symbionts.

Aphid thermal tolerance is governed by a point mutation in bacterial symbionts.
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DOI:
10.1371/journal.pbio.0050096
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发表时间:
2007-05
期刊:
影响因子:
9.8
通讯作者:
Moran NA
Moran NA
中科院分区:
生物学1区
文献类型:
--
作者:
Dunbar HE;Wilson AC;Ferguson NR;Moran NA

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共生是一种普遍存在的现象,它产生生物复杂性,影响适应并扩大生态能力。然而,共生体可能受到克隆性和基因组退化等遗传限制,也会对宿主产生限制。专性共生的模型是蚜虫和 Buchnera aphidicola 细菌之间的模型,该细菌提供必需的营养。我们报告了蚜虫 Acyrthosiphon pisum 的 Buchnera 突变,该突变在实验室品系中反复出现,并在田间种群中发生。这种单核苷酸缺失会影响 ibpA 热休克转录启动子内的同聚运行,编码一个小的热休克蛋白。这种 Buchnera 突变实际上消除了 ibpA 对热应激的转录反应,甚至在凉爽或中等温度下也降低了其表达。此外,这种共生体突变以依赖于热环境的方式极大地影响宿主的适应性。在幼虫时期经历短暂的热暴露后,携带短等位基因共生体的蚜虫很少或没有产生后代,并且几乎不含 Buchnera,与携带未缺失的共生体的蚜虫形成鲜明对比。相反,在持续凉爽的条件下,含有短等位基因共生体的蚜虫繁殖更早,并保持更高的繁殖率。短等位基因在野外种群中具有相当高的频率(高达 20%),进一步支持了以下观点:在某些条件下,降低 ibpA 表达可以改善宿主的适应性。这种反复出现的 Buchnera 突变控制着蚜虫宿主的耐热性。由于共生细菌的高突变率及其在宿主代谢和发育中的关键作用,共生微进化对宿主生态耐受性产生重大影响的其他情况可能很普遍。蚜虫是一种以汁液为食的昆虫,依靠 Buchnera 属的专性细菌共生体来生物合成所需的营养物质。通过研究豌豆蚜中的 Buchnera 基因表达,我们发现了小热休克蛋白 ibpA 的转录启动子中的重复突变(单碱基缺失)。这种突变在实验室中从单个雌性蚜虫衍生的亚系中出现并被固定两次,并保持在 20°C 恒定温度。使用仅存在 Buchnera 突变的蚜虫品系进行的实验表明,它消除了 ibpA 对热休克的转录反应,并影响 ibpA 在低温下的表达。在含有 Buchnera 突变的蚜虫中,幼虫时期的短暂热处理会导致大部分或全部共生体消失并导致繁殖失败;同样的处理对含有Buchnera但没有突变的蚜虫效果不大。相反,在持续较低的温度下,携带这种突变的 Buchnera 蚜虫享有繁殖优势。豌豆蚜种群具有 Buchnera 突变的多态性,这表明它通过选择而保持在相当高的频率。这项研究表明,专性共生体的突变会对宿主的适应性和地理分布产生重大影响。豌豆蚜 (Acyrthosiphon pisum) 的细菌 Buchnera 共生体中热休克转录启动子中反复出现的单核苷酸缺失会以热依赖性方式显着影响宿主的适应性。
Symbiosis is a ubiquitous phenomenon generating biological complexity, affecting adaptation, and expanding ecological capabilities. However, symbionts, which can be subject to genetic limitations such as clonality and genomic degradation, also impose constraints on hosts. A model of obligate symbiosis is that between aphids and the bacterium Buchnera aphidicola, which supplies essential nutrients. We report a mutation in Buchnera of the aphid Acyrthosiphon pisum that recurs in laboratory lines and occurs in field populations. This single nucleotide deletion affects a homopolymeric run within the heat-shock transcriptional promoter for ibpA, encoding a small heat-shock protein. This Buchnera mutation virtually eliminates the transcriptional response of ibpA to heat stress and lowers its expression even at cool or moderate temperatures. Furthermore, this symbiont mutation dramatically affects host fitness in a manner dependent on thermal environment. Following a short heat exposure as juveniles, aphids bearing short-allele symbionts produced few or no progeny and contained almost no Buchnera, in contrast to aphids bearing symbionts without the deletion. Conversely, under constant cool conditions, aphids containing symbionts with the short allele reproduced earlier and maintained higher reproductive rates. The short allele has appreciable frequencies in field populations (up to 20%), further supporting the view that lowering of ibpA expression improves host fitness under some conditions. This recurring Buchnera mutation governs thermal tolerance of aphid hosts. Other cases in which symbiont microevolution has a major effect on host ecological tolerance are likely to be widespread because of the high mutation rates of symbiotic bacteria and their crucial roles in host metabolism and development. Aphids are sap-feeding insects that depend on obligate bacterial symbionts of the genus Buchnera for biosynthesis of needed nutrients. Studying Buchnera gene expression in pea aphids, we identified a recurring mutation (a single-base deletion) in the transcriptional promoter of the small heat-shock protein, ibpA. This mutation arose and was fixed twice in sublines derived from a single female aphid in the lab and kept at constant 20 °C. Experiments using aphid lines that differed only in the presence of this Buchnera mutation revealed that it eliminates the ibpA transcriptional response to heat shock and affects ibpA expression at low temperatures. In aphids containing Buchnera with the mutation, a short heat treatment as juveniles leads to elimination of most or all symbionts and to reproductive failure; the same treatment has little effect on aphids containing Buchnera without the mutation. Conversely, at constant lower temperatures, aphids with Buchnera bearing this mutation enjoy a reproductive advantage. Pea aphid populations are polymorphic for the Buchnera mutation, suggesting that it is maintained at substantial frequencies by selection. This study indicates that mutations in obligate symbionts can have major consequences for host fitness and geographic distributions. A recurring single-nucleotide deletion in a heat-shock transcriptional promoter in the bacterialBuchnera symbiont of the pea aphid(Acyrthosiphon pisum) dramatically affects host fitness in a thermal-dependent manner.
DOI: 10.1046/j.1365-2311.2002.00393.x
发表时间: 2002-04-01
影响因子: 2.2
作者:
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发表时间: 2006-09-22
期刊: SCIENCE
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作者:
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发表时间: 2002-08-01
期刊: MICROBIAL ECOLOGY
影响因子: 3.6
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发表时间: 2005-11-22
影响因子: 11.1
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