Ibarra-Juarez L A, Burton M A J, Biedermann P H W, Cruz L, Desgarennes D, Ibarra-Laclette E, Latorre A, Alonso-Sánchez A, Villafan E, Hanako-Rosas G, López L, Vázquez-Rosas-Landa M, Carrion G, Carrillo D, Moya A, Lamelas A
Red de Estudios Moleculares Avanzados, Instituto de Ecología A. C., Xalapa, México.
Chair of Forest Entomology and Protection, University of Freiburg, Freiburg, Germany.
mSystems. 2020 Sep 15;5(5):e00541-20. doi: 10.1128/mSystems.00541-20.
The bacterial and fungal community involved in ambrosia beetle fungiculture remains poorly studied compared to the famous fungus-farming ants and termites. Here we studied microbial community dynamics of laboratory nests, adults, and brood during the life cycle of the sugarcane shot hole borer, We identified a total of 40 fungal and 428 bacterial operational taxonomic units (OTUs), from which only five fungi (a fungus and four ascomycete yeasts) and four bacterial genera (, , , and ) can be considered the core community playing the most relevant symbiotic role. Both the fungal and bacterial populations varied significantly during the beetle's life cycle. While the ascomycete yeasts were the main colonizers of the gallery early on, the and other filamentous fungi appeared after day 10, at the time when larval hatching happened. Regarding bacteria, and dominated overall but decreased in foundresses and brood with age. Finally, inferred analyses of the putative metabolic capabilities of the bacterial microbiome revealed that they are involved in (i) degradation of fungal and plant polymers, (ii) fixation of atmospheric nitrogen, and (iii) essential amino acid, cofactor, and vitamin provisioning. Overall, our results suggest that yeasts and bacteria are more strongly involved in supporting the beetle-fungus farming symbiosis than previously thought. Ambrosia beetles farm their own food fungi within tunnel systems in wood and are among the three insect lineages performing agriculture (the others are fungus-farming ants and termites). In ambrosia beetles, primary ambrosia fungus cultivars have been regarded essential, whereas other microbes have been more or less ignored. Our KEGG analyses suggest so far unknown roles of yeasts and bacterial symbionts, by preparing the tunnel walls for the primary ambrosia fungi. This preparation includes enzymatic degradation of wood, essential amino acid production, and nitrogen fixation. The latter is especially exciting because if it turns out to be present in ambrosia beetles, all farming animals (including humans) are dependent on atmospheric nitrogen fertilization of their crops. As previous internal transcribed spacer (ITS) metabarcoding approaches failed on covering the primary ambrosia fungi, our 18S metabarcoding approach can also serve as a template for future studies on the ambrosia beetle-fungus symbiosis.
与著名的培育真菌的蚂蚁和白蚁相比，参与食菌小蠹虫真菌养殖的细菌和真菌群落仍未得到充分研究。在这里，我们研究了甘蔗小蠹虫生命周期中实验室巢穴、成虫和幼虫的微生物群落动态。我们总共鉴定出40个真菌和428个细菌可操作分类单元（OTU），其中只有五种真菌（一种担子菌和四种子囊菌酵母）和四个细菌属（、、和）可被视为发挥最相关共生作用的核心群落。在小蠹虫的生命周期中，真菌和细菌种群均有显著变化。虽然子囊菌酵母在早期是虫道的主要定殖者，但和其他丝状真菌在第10天后出现，此时幼虫孵化。关于细菌，和总体上占主导地位，但在雌虫和幼虫中随年龄增长而减少。最后，对细菌微生物组假定代谢能力的推断分析表明，它们参与了（i）真菌和植物聚合物的降解，（ii）大气氮的固定，以及（iii）必需氨基酸、辅因子和维生素的供应。总体而言，我们的结果表明，酵母和细菌在支持小蠹虫 - 真菌养殖共生关系方面比以前认为的更为重要。食菌小蠹虫在木材的隧道系统中培育自己的食用真菌，是进行农业活动的三个昆虫谱系之一（另外两个是培育真菌的蚂蚁和白蚁）。在食菌小蠹虫中，主要的共生真菌品种被认为是必不可少的，而其他微生物或多或少被忽视了。我们的KEGG分析表明，酵母和细菌共生体目前未知的作用是为主要共生真菌准备虫道壁。这种准备工作包括木材的酶促降解、必需氨基酸的产生和氮的固定。后者尤其令人兴奋，因为如果事实证明食菌小蠹虫中存在这种情况，那么所有从事农业养殖的动物（包括人类）的作物都依赖于大气氮的施肥。由于以前的内转录间隔区（ITS）宏条形码方法未能覆盖主要的共生真菌，我们的18S宏条形码方法也可以作为未来食菌小蠹虫 - 真菌共生关系研究的模板。
