Entomology, Max Planck Institute for Chemical Ecology, Hans-Knoell-Str. 8, 07745, Jena, Germany.
INRA, Université Côte d'Azur, CNRS, ISA, Sophia Antipolis, France.
BMC Evol Biol. 2019 May 10;19(1):100. doi: 10.1186/s12862-019-1429-9.
Cellulose, a major polysaccharide of the plant cell wall, consists of β-1,4-linked glucose moieties forming a molecular network recalcitrant to enzymatic breakdown. Although cellulose is potentially a rich source of energy, the ability to degrade it is rare in animals and was believed to be present only in cellulolytic microbes. Recently, it has become clear that some animals encode endogenous cellulases belonging to several glycoside hydrolase families (GHs), including GH45. GH45s are distributed patchily among the Metazoa and, in insects, are encoded only by the genomes of Phytophaga beetles. This study aims to understand both the enzymatic functions and the evolutionary history of GH45s in these beetles.
To this end, we biochemically assessed the enzymatic activities of 37 GH45s derived from five species of Phytophaga beetles and discovered that beetle-derived GH45s degrade three different substrates: amorphous cellulose, xyloglucan and glucomannan. Our phylogenetic and gene structure analyses indicate that at least one gene encoding a putative cellulolytic GH45 was present in the last common ancestor of the Phytophaga, and that GH45 xyloglucanases evolved several times independently in these beetles. The most closely related clade to Phytophaga GH45s was composed of fungal sequences, suggesting this GH family was acquired by horizontal gene transfer from fungi. Besides the insects, other arthropod GH45s do not share a common origin and appear to have emerged at least three times independently.
The rise of functional innovation from gene duplication events has been a fundamental process in the evolution of GH45s in Phytophaga beetles. Both, enzymatic activity and ancestral origin suggest that GH45s were likely an essential prerequisite for the adaptation allowing Phytophaga beetles to feed on plants.
纤维素是植物细胞壁的主要多糖，由β-1,4 键连接的葡萄糖单元组成，形成对酶分解具有抗性的分子网络。尽管纤维素是一种潜在的丰富能源，但动物分解纤维素的能力很少见，据信仅存在于纤维素分解微生物中。最近，人们清楚地认识到，一些动物编码属于几种糖苷水解酶家族（GH）的内源性纤维素酶，包括 GH45。GH45 在后生动物中分布不均，在昆虫中，仅由 Phytophaga 甲虫的基因组编码。本研究旨在了解这些甲虫中 GH45 的酶学功能和进化历史。
为此，我们对来自 5 种 Phytophaga 甲虫的 37 种 GH45 进行了生化评估，发现甲虫衍生的 GH45 可降解三种不同的底物：无定形纤维素、木葡聚糖和葡甘露聚糖。我们的系统发育和基因结构分析表明，至少有一种编码潜在纤维素水解 GH45 的基因存在于 Phytophaga 的最后共同祖先中，并且这些甲虫中 GH45 木葡聚糖酶独立进化了多次。与 Phytophaga GH45 最密切相关的分支由真菌序列组成，表明该 GH 家族是通过水平基因转移从真菌中获得的。除了昆虫，其他节肢动物 GH45 没有共同的起源，似乎至少独立出现了三次。
功能创新的出现源于基因复制事件，这是 Phytophaga 甲虫 GH45 进化的基本过程。酶学活性和起源都表明，GH45 可能是允许 Phytophaga 甲虫以植物为食的适应的必要前提。
