The complete mitogenome of the springtail Tullbergia bisetosa: a subterranean springtail from the sub-Antarctic region

Abstract

Tullbergia bisetosa is a springtail (Collembola) native to the sub-Antarctic Prince Edward Islands. Unlike most other springtails, it has acquired a euedaphic (living within the soil) life form. In the present study, the complete mitogenome of T. bisetosa was sequenced. It has a length of 15,204 bp and comprises 13 protein-coding genes, 22 tRNAs, and two rRNAs. The mitogenome has the following base composition: A = 35.5%, T = 32.3%, G = 10.6%, and C = 21.1%. A Bayesian phylogenetic tree shows that T. bisetosa is grouped with springtails that possess similar morphological features and similar life histories. Our results suggest a mitogenomic signal towards morphological traits that conforms to a euedaphic lifestyle.

Keywords:

• Mitogenome
• Tullbergia bisetosa
• soil ecosystems
• Collembola
• sub-Antarctic
• Prince Edward Islands

Collembola (springtails) are a ubiquitous and widespread group of arthropods that inhabit a wide range of terrestrial ecosystems, although the choice of habitat varies between different species (Hopkin 1997). Springtails are macroscopic and wingless, and most species that are epidaphic (living in surface vegetation) possess a furca (springing organ) which facilitates their dispersal (Hopkin 1997). However, some springtails deviate from the norm and have adapted to different ecological niches. A case in hand is Tullbergia bisetosa Börner 1902 which has acquired a euedaphic life form (living deep within the soil). This species is blind, has reduced appendages, lacks a furca, and is likely parthenogenic during stable environmental conditions, which changes to sexual reproduction when conditions become unfavourable (Chahartaghi et al. 2009; Chernova et al. 2010). Here, we present the complete mitogenome of T. bisetosa and investigate its phylogenetic placement among other springtails with different morphological features and habitat preferences.

Genomic DNA was extracted from 16 individuals collected from the Prince Edward Islands (46.767°S, 37.850°E) using the DNeasy Blood and Tissue Kit (Qiagen^®, Germany). DNA from one of these specimens has been deposited at the Iziko Museum, Cape Town, voucher number SAM-ENW-C010313. Genomic libraries were prepared and sequenced using the Illumina HiSeq4000 sequencer (Illumina, USA). The software package NOVOPlasty v2.7.2 (Dierckxsens et al. 2017) was used to assemble the mitogenome. The program’s default settings were used, except for the insert size, which was changed to 350 bp corresponding to the genomic library preparation pipeline. The starting seed for the assembly was the cytochrome c oxidase subunit I gene of T. bisetosa (Myburgh et al. 2007; Accession No. DQ147448). The MITOS WebServer (Bernt et al. 2013) was used for the initial annotation, and sequence boundaries of the protein-coding genes (PCGs) and ribosomal RNAs were confirmed using Exonerate v2.2 (Slater and Birney 2005) and Infernal v1.1 (Nawrocki and Eddy 2013).

The PCGs of T. bisetosa and nine other closely related species (sequence identity >69%) were independently aligned and a consensus Bayesian phylogenetic tree of all 13 PCGs was constructed in BEAST v2.5 (Bouckaert et al. 2014) selecting the HKY substitution model (Hasegawa et al. 1985), 300 million MCMC iterations, and a 33% burnin. The phylogenetic tree was visualized in Figtree v1.4.3 (Rambaut 2016) (Figure 1).

Figure 1. A Bayesian phylogenetic tree of Tullbergia bisetosa and nine other species (six Collembola and three outgroup taxa). The following species were used for the phylogenetic analysis: Tullbergia bisetosa MK520870, Tetrodontophora bielanensis AF272824, Friesea grisea EU124719, Gomphiocephalus hodgsoni NC_005438, Cryptopygus antarcticus NC_010533, Cryptopygus terranovus NC_037610, Orchesella villosa EU016195, Anopheles funestus MG742199, Sabethes belisarioi NC_037498, and Zeugodacus tau MF966383. The posterior probabilities are at each node.

The circularized mitogenome consists of 15,204 bp with the base composition of A = 35.5%, T = 32.3%, G = 10.6%, and C = 21.1%. We observed several occurrences of non-canonical initiation and truncated stop codons (TNN), and a low GC content, both of which are common in invertebrates (Donath et al. in press; Tikole and Sankararamakrishnan 2006).

The Bayesian phylogenetic tree recovered T. bisetosa and Tetradontophora bielanensis as sister taxa within a monophyletic clade that comprises other euedaphic springtails, Friesea grisea and Gomphiocephalus hodgsoni. The current phylogeny supports a single origin for the euedaphic lifestyle in Collembola. The epidaphic springtails (Cryptopygus antarcticus, Cryptopygus terranovus, and Orchesella villosa) form a separate clade (see also Monsanto et al. 2019). Since mitochondrial DNA is involved in thermal and anaerobic respiratory adaptations (Silva et al. 2014), the current study emphasises that mitogenomes may be under selection for traits that are critical for a euedaphic lifestyle.

Acknowledgements

Specimens were collected under Prince Edward research permits granted by the Department of Environmental Affairs (DEA) (permit number 1/2013). The DEA is acknowledged for logistical support. We acknowledge the Centre for High Performance Computing (CHPC) in Cape Town and the University of Johannesburg’s IT services for bioinformatics support.

Disclosure statement

The authors have reported no conflict of interest, and are responsible for the content and writing of this article.

Additional information

Funding

The authors acknowledge the National Research Foundation (NRF SANAP grant to BvV: grant number 110728) and the University of Johannesburg for the Global Excellence and Stature postdoctoral fellowship awarded to A.E.-K.