The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.

The genome sequence of the leaf-cutter ant Atta cephalotes reveals insights into its obligate symbiotic lifestyle.
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DOI:
10.1371/journal.pgen.1002007
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发表时间:
2011-02-10
期刊:
影响因子:
4.5
通讯作者:
Currie CR
Currie CR
中科院分区:
生物学2区
文献类型:
--
作者:
Suen G;Teiling C;Li L;Holt C;Abouheif E;Bornberg-Bauer E;Bouffard P;Caldera EJ;Cash E;Cavanaugh A;Denas O;Elhaik E;Favé MJ;Gadau J;Gibson JD;Graur D;Grubbs KJ;Hagen DE;Harkins TT;Helmkampf M;Hu H;Johnson BR;Kim J;Marsh SE;Moeller JA;Muñoz-Torres MC;Murphy MC;Naughton MC;Nigam S;Overson R;Rajakumar R;Reese JT;Scott JJ;Smith CR;Tao S;Tsutsui ND;Viljakainen L;Wissler L;Yandell MD;Zimmer F;Taylor J;Slater SC;Clifton SW;Warren WC;Elsik CG;Smith CD;Weinstock GM;Gerardo NM;Currie CR

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切叶蚂蚁是新热带地区最重要的食草性昆虫之一,它采集大量的新鲜叶片材料。蚂蚁用树叶培养一种真菌,作为蚁群的主要食物来源。这种专属的蚂蚁-真菌互惠关系是少数非人类耕作的例子之一,很可能促进了它们巨大殖民地的形成。成熟的切叶蚂蚁群体包含数以百万计大小不等的工蚁,从小型园丁到大型士兵,导致蚂蚁内最复杂的多态种姓系统之一。为了开始揭示这个系统的基因组基础,我们使用454焦磷酸测序法对白头翁的基因组进行了测序。从这只蚂蚁的生活方式中预测到,它已经经历了基因改造,这反映了它对真菌营养的专属依赖。对这一基因组序列的分析与这一假设是一致的,因为我们发现了与营养获取相关的基因减少的证据。这些包括丝氨酸蛋白酶的大量减少(这可能是不必要的,因为蛋白质分解不是处理从真菌获得的营养的主要机制),参与精氨酸生物合成的基因丢失(表明这种氨基酸是从真菌获得的),以及缺乏六丝氨酸(在其他昆虫的幼虫发育期间隔离氨基酸)。在最近关于其他昆虫的基因组序列与有益微生物共生的报道之后,头蚁基因组为了解这种蚂蚁的共生生活方式提供了新的见解,并促进了我们对宿主-微生物共生的理解。切叶蚂蚁的工作人员寻找和切割树叶,他们用这些树叶来支持一种特殊的真菌的生长,这种真菌是蚂蚁群体的主要食物来源。这些蚂蚁自己种植食物的能力可能有助于它们成为新大陆热带生态系统中最具优势的食草动物之一,在热带生态系统中,切叶蚂蚁收获的植物生物量比其他任何食草动物物种都多。这些蚂蚁还进化出了一种最复杂的分工形式,由专门从事不同任务的不同大小的工蚁组成的蚁群。为了深入了解这些蚂蚁的生物学,我们对切叶蚂蚁Atta cephalotes的第一个基因组进行了测序。我们对这个基因组的分析揭示了这些蚂蚁对真菌的固有营养依赖的特征。这些发现是切叶蚂蚁获取营养能力降低的第一个遗传学证据,这可能是由它们的真菌共生体补偿的。这些发现与其他营养宿主-微生物共生现象平行,表明在这些类型的关联中存在趋同的基因组修改。
Leaf-cutter ants are one of the most important herbivorous insects in the Neotropics, harvesting vast quantities of fresh leaf material. The ants use leaves to cultivate a fungus that serves as the colony's primary food source. This obligate ant-fungus mutualism is one of the few occurrences of farming by non-humans and likely facilitated the formation of their massive colonies. Mature leaf-cutter ant colonies contain millions of workers ranging in size from small garden tenders to large soldiers, resulting in one of the most complex polymorphic caste systems within ants. To begin uncovering the genomic underpinnings of this system, we sequenced the genome of Atta cephalotes using 454 pyrosequencing. One prediction from this ant's lifestyle is that it has undergone genetic modifications that reflect its obligate dependence on the fungus for nutrients. Analysis of this genome sequence is consistent with this hypothesis, as we find evidence for reductions in genes related to nutrient acquisition. These include extensive reductions in serine proteases (which are likely unnecessary because proteolysis is not a primary mechanism used to process nutrients obtained from the fungus), a loss of genes involved in arginine biosynthesis (suggesting that this amino acid is obtained from the fungus), and the absence of a hexamerin (which sequesters amino acids during larval development in other insects). Following recent reports of genome sequences from other insects that engage in symbioses with beneficial microbes, the A. cephalotes genome provides new insights into the symbiotic lifestyle of this ant and advances our understanding of host–microbe symbioses. Leaf-cutter ant workers forage for and cut leaves that they use to support the growth of a specialized fungus, which serves as the colony's primary food source. The ability of these ants to grow their own food likely facilitated their emergence as one of the most dominant herbivores in New World tropical ecosystems, where leaf-cutter ants harvest more plant biomass than any other herbivore species. These ants have also evolved one of the most complex forms of division of labor, with colonies composed of different-sized workers specialized for different tasks. To gain insight into the biology of these ants, we sequenced the first genome of a leaf-cutter ant, Atta cephalotes. Our analysis of this genome reveals characteristics reflecting the obligate nutritional dependency of these ants on their fungus. These findings represent the first genetic evidence of a reduced capacity for nutrient acquisition in leaf-cutter ants, which is likely compensated for by their fungal symbiont. These findings parallel other nutritional host–microbe symbioses, suggesting convergent genomic modifications in these types of associations.
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