Data from: Analysis of the genome of the New Zealand giant collembolan (Holacanthella duospinosa) sheds light on hexapod evolution

Background: The New Zealand collembolan genus Holacanthella contains the largest species of springtails (Collembola) in the world. Using Illumina technology we have sequenced and assembled a draft genome and transcriptome from Holacanthella duospinosa (Salmon). We have used this annotated assembly to investigate the genetic basis of a range of traits critical to the evolution of the Hexapoda, the phylogenetic position of H. duospinosa and potential horizontal gene transfer events.

Results: Our genome assembly was ~375 Mbp in size with a scaffold N50 of ~230 Kbp and sequencing coverage of ~180×. DNA elements, LTRs and simple repeats and LINEs formed the largest components and SINEs were very rare. Phylogenomics (370,877 amino acids) placed H. duospinosa within the Neanuridae. We recovered orthologs of the conserved sex determination genes thought to play a role in sex determination. Analysis of CpG content suggested the absence of DNA methylation, and consistent with this we were unable to detect orthologs of the DNA methyltransferase enzymes. The small subunit rRNA gene contained a possible retrotransposon. The Hox gene complex was broken over two scaffolds. For chemosensory ability, at least 15 and 18 ionotropic glutamate and gustatory receptors were identified, respectively. However, we were unable to identify any odorant receptors or their obligate co-receptor Orco. Twenty-three chitinase-like genes were identified from the assembly. Members of this multigene family may play roles in the digestion of fungal cell walls, a common food source for these saproxylic organisms. We also detected 59 and 96 genes that blasted to bacteria and fungi, respectively, but were located on scaffolds that otherwise contained arthropod genes.

Conclusions: The genome of H. duospinosa contains some unusual features including a Hox complex broken over two scaffolds, in a different manner to other arthropod species, a lack of odorant receptor genes and an apparent lack of environmentally responsive DNA methylation, unlike many other arthropods. Our detection of candidate horizontal gene transfer candidates confirms that this phenomenon is occurring across Collembola. These findings allow us to narrow down the regions of the arthropod phylogeny where key innovations have occurred that have facilitated the evolutionary success of Hexapoda.

背景：新西兰弹尾目（Collembola）棘跳虫属（Holacanthella）包含全球体型最大的弹尾虫（springtails）物种。本研究利用Illumina测序技术（Illumina）对双刺棘跳虫（Holacanthella duospinosa, Salmon）的草稿基因组与转录组进行了测序与组装。借助该注释后的组装序列，我们探究了六足动物（Hexapoda）演化相关的一系列关键性状的遗传基础、双刺棘跳虫的系统发育位置，以及潜在的水平基因转移（horizontal gene transfer）事件。

结果：本研究获得的基因组组装序列总长约375 Mbp，支架N50（scaffold N50）约230 Kbp，测序覆盖度约180×。DNA元件、长末端重复序列（long terminal repeat, LTR）、简单重复序列以及长散在核元件（long interspersed nuclear elements, LINE）构成了基因组的主要组成部分，而短散在核元件（short interspersed nuclear elements, SINE）则极为罕见。基于370877个氨基酸序列的系统发育基因组学（phylogenomics）分析将双刺棘跳虫归入新跳虫科（Neanuridae）。我们鉴定得到了保守性别决定基因的直系同源基因（ortholog），这类基因被认为在性别决定过程中发挥功能。CpG含量分析显示该物种不存在DNA甲基化（DNA methylation），与此一致的是，我们未能检测到DNA甲基转移酶（DNA methyltransferase）的直系同源基因。其小亚基rRNA基因中含有一个潜在的逆转录转座子（retrotransposon）。Hox基因簇（Hox gene complex）被拆分至两个支架序列上。在化学感应能力方面，我们分别鉴定得到至少15个离子型谷氨酸受体（ionotropic glutamate receptor）与18个味觉受体（gustatory receptor），但未能检测到任何嗅觉受体（odorant receptor）及其必需共受体Orco的序列。本组装序列中共鉴定得到23个几丁质酶样基因（chitinase-like gene），该多基因家族的成员可能参与真菌细胞壁的降解——而真菌正是这类腐生生物（saproxylic organisms）的常见食物来源。我们还分别检测到59个与细菌、96个与真菌同源的基因，但这些基因所在的支架序列中同时包含节肢动物（arthropod）基因。

结论：双刺棘跳虫的基因组存在若干非同寻常的特征：其一，Hox基因簇以不同于其他节肢动物的方式被拆分至两个支架序列上；其二，缺失嗅觉受体基因；其三，与多数其他节肢动物不同，该物种似乎不存在环境响应型DNA甲基化。我们对候选水平基因转移事件的检测结果证实，这一现象广泛存在于弹尾目类群中。本研究结果帮助我们缩小了节肢动物系统发育树中关键创新事件的发生范围，这些创新事件正是推动六足动物演化成功的关键。