DeMilto Alexandria M, Rouquette Monte, Mueller Ulrich G, Kellner Katrin, Seal Jon N
Department of Biology, University of Texas at Tyler, 3900 University Blvd, Tyler, TX 75799, USA.
Texas Agricultural Experiment Station, Texas A&M University Agricultural Research and Extension Center at Overton, Overton, TX 75684, USA.
J Insect Physiol. 2017 Apr;98:301-308. doi: 10.1016/j.jinsphys.2017.02.001. Epub 2017 Feb 11.
Fungus-gardening or attine ants have outsourced most of their digestive function to a symbiotic fungus. The ants feed their fungus - essentially an external digestive organ - a variety of substrates of botanical origin, including fresh and dried flowers, leaves and insect frass (processed leaves). Although plant tissues are rich in fibers (lignocelluloses, hemicelluloses, pectins and starches) and the symbiotic fungus possesses the genetic and enzymatic machinery to metabolize these compounds, the highly derived attines, the leaf-cutters (Atta and Acromyrmex), are known to produce fiber-rich waste. While leaf-cutting ants are important consumers of primary plant tissue, there have been fewer studies on physiological activity of fungi grown by closely related ant species in the genus Trachymyrmex, which generally grow related species of fungi, have smaller colonies and consume a wider variety of fungal substrates in addition to fresh leaves and flowers. In this study, we measured the cellulase activity of the fungus-gardening ants Atta texana, Trachymyrmex arizonensis and T. septentrionalis. We then quantified fiber consumption of the fungus-gardening ants Trachymyrmex septentrionalis and Trachymyrmex arizonensis by comparing the amounts and percentages present in their food and in fungus garden refuse during a controlled feeding experiment over the span of several months. Finally, we compared waste composition of T. arizonensis colonies growing different fungal strains, because this species is known to cultivate multiple strains of Leucoagaricus in its native range. The leaf-cutting ant A. texana was found to have lower cellulytic activity than T. arizonensis or T. septentrionalis. Total lignocellulose and hemicellulose amounts were significantly lower in refuse piles than in the substrates fed to the Trachymyrmex colonies, thus these fibers were consumed by the fungal symbionts of these ant species. Although lignocellulose utilization was similar in two distinct fungal species grown by T. arizonensis colonies, hemicellulose utilization was higher in T. arizonensis colonies growing a derived leaf-cutting ant fungal symbiont than when growing a native type of symbiont. The results of this study demonstrate that fiber digestion in fungus-gardening ants is an outcome of ant-fungal interaction.
培育真菌的蚂蚁,即阿蒂纳蚁,已将其大部分消化功能外包给了一种共生真菌。蚂蚁为它们的真菌——本质上是一个外部消化器官——提供各种植物源底物,包括鲜花、干花、树叶和昆虫粪便(加工过的树叶)。尽管植物组织富含纤维(木质纤维素、半纤维素、果胶和淀粉),且共生真菌拥有代谢这些化合物的基因和酶机制,但高度特化的阿蒂纳蚁,即切叶蚁(切叶蚁属和顶切叶蚁属),却会产生富含纤维的废物。虽然切叶蚁是初级植物组织的重要消费者,但对于近缘的曲颊蚁属蚂蚁所培育真菌的生理活性研究较少,曲颊蚁属通常培育相关真菌物种,蚁群规模较小,除了新鲜树叶和花朵外,还消耗更多种类的真菌底物。在本研究中,我们测量了培育真菌的德克萨斯切叶蚁、亚利桑那曲颊蚁和北方曲颊蚁的纤维素酶活性。然后,通过比较在为期数月的对照饲养实验中,北方曲颊蚁和亚利桑那曲颊蚁食物及真菌园废弃物中的纤维含量和百分比,我们对它们的纤维消耗量进行了量化。最后,我们比较了培育不同真菌菌株的亚利桑那曲颊蚁蚁群的废物组成,因为已知该物种在其原生范围内培育多种亮白蘑菇菌株。研究发现,德克萨斯切叶蚁的纤维素分解活性低于亚利桑那曲颊蚁或北方曲颊蚁。曲颊蚁属蚁群的废弃物堆中,木质纤维素和半纤维素的总量显著低于喂食给它们的底物,因此这些纤维被这些蚂蚁物种的真菌共生体消耗了。虽然亚利桑那曲颊蚁蚁群培育的两种不同真菌物种对木质纤维素的利用率相似,但培育源自切叶蚁的真菌共生体的亚利桑那曲颊蚁蚁群对半纤维素的利用率高于培育原生类型共生体时的利用率。本研究结果表明,培育真菌的蚂蚁对纤维的消化是蚂蚁与真菌相互作用的结果。