- Research article
- Open Access
The mitochondrial genomes of sarcoptiform mites: are any transfer RNA genes really lost?
BMC Genomics volume 19, Article number: 466 (2018)
Mitochondrial (mt) genomes of animals typically contain 37 genes for 13 proteins, two ribosomal RNA (rRNA) genes and 22 transfer RNA (tRNA) genes. In sarcoptiform mites, the entire set of mt tRNA genes is present in Aleuroglyphus ovatus, Caloglyphus berlesei, Dermatophagoides farinae, D. pteronyssinus, Histiostoma blomquisti and Psoroptes cuniculi. Loss of 16 mt tRNA genes, however, was reported in Steganacarus magnus; loss of 2–3 tRNA genes was reported in Tyrophagus longior, T. putrescentiae and Sarcoptes scabiei. Nevertheless, convincing evidence for mt gene loss is lacking in these mites.
We sequenced the mitochondrial genomes of two sarcoptiform mites, Histiostoma feroniarum (13,896 bp) and Rhizoglyphus robini (14,244 bp). Using tRNAScan and ARWEN programs, we identified 16 and 17 tRNA genes in the mt genomes of H. feroniarum and R. robini, respectively. The other six mt tRNA genes in H. feroniarum and five mt tRNA genes in R. robini can only be identified manually by sequence comparison when alternative anticodons are considered. We applied this manual approach to other mites that were reported previously to have lost mt tRNA genes. We were able to identify all of the 16 mt tRNA genes that were reported as lost in St. magnus, two of the three mt tRNA genes that were reported as lost in T. longior and T. putrescentiae, and the two mt tRNA genes that were reported as lost in Sa. scabiei. All of the tRNA genes inferred from these manually identified genes have truncation in the arms and mismatches in the stems.
Our results reveal very unconventional tRNA structures in sarcoptiform mites and do not support the loss of mt tRNA genes in these mites. The functional implication of the drastic structural changes in these tRNA genes remains to be investigated.
Mitochondria are critical organelles for cellular energy production in eukaryotes. The four protein complexes in the respiratory chain are encoded by both mitochondrial (mt) genomes and nuclear genomes . For animals, mt genomes typically have 37 genes for 13 proteins, two ribosomal RNA (rRNA) genes and 22 transfer RNA (tRNA) genes . The proteins are essential for the formation of respiratory chain, and the rRNA genes and tRNA genes are essential for the translation process. Loss of genes is rare in animal mt genomes, but has been reported or suggested in several lineages, e.g., loss of atp8 in nematodes , bivalves , cnidarians  and flatworms , loss of trnD in scorpions , and loss of both protein-coding and tRNA genes in mites [8, 9].
Mites and ticks (subclass Acari) represent a major group (> 54,000 species) in the class Arachnida  and colonize a wide range of terrestrial, marine and aquatic habitats . The order Sarcoptiformes comprises approximately 16,300 extant species . Some species are medically important, e.g. house dust mites causing allergic symptoms in humans [13, 14], scabies mite infecting skin of humans and other animal species . Some species are also economically important, e.g. acarid mites inhabiting stored food products . Mt. genomes of 40 species of mites and 48 species of ticks have been sequenced (as of records from database of NCBI on 1 August 2017). Loss of mt tRNA genes has been reported in four sarcoptiform mites from three superfamilies: 16 in Steganacarus magnus (Phthiracaroidea) , three (trnF, trnS 1 and trnQ) in two Tyrophagus species (Acaroidea) [17, 18], and two (trnA and trnY) in Sarcoptes scabiei (Sarcoptoidea) . Edwards et al. reanalyzed the mt genome sequence of St. magnus and identified three of the 16 tRNA genes reported as lost . On the other hand, the full set of tRNA genes were found in six other species of sarcoptiform mites from four superfamilies: Aleuroglyphus ovatus , Caloglyphus berlesei , Dermatophagoides farinae , D. pteronyssinus , Histiostoma blomquisti  and Psoroptes cuniculi . Thus, the evidence available is conflicting whether or not any tRNA genes are really lost in sarcoptiform mites. If tRNA genes were indeed lost, to what extent did it occur? If no tRNA genes were lost, why couldn’t they be identified in some sarcoptiform mites? To address these questions and to lay a solid foundation for comparative studies of the mt genomes of sarcoptiform mites, we sequenced the mt genomes of two more species of sarcoptiform mites, Rhizoglyphus robini and Histiostoma feroniarum, from the superfamilies Acaroidea and Histiostomatoidea respectively, and compared the mt genome sequences of all of the sarcoptiform mites available to date.
Mitochondrial genomes of Rhizoglyphus robini and Histiostoma feroniarum
The mt genomes of R. robini and H. feroniarum are 14,244 bp and 13,896 bp long, respectively. Like other mites and ticks reported previously, the mt genomes of R. robini and H. feroniarum are circular and have the 13 protein-coding genes (PCGs) and two rRNA genes (Fig. 1, Additional file 1: Figure S1, Additional file 2: Table S1 and Additional file 3: Table S2). Using tRNAscan-SE  and ARWEN  programs, we identified 16 and 17 tRNA genes in the mt genomes of H. feroniarum and R. robini. The other six mt tRNA genes of H. feroniarum (trnR, trnM, trnS 2 , trnY, trnS 1 , trnA) and the other five mt tRNA genes of R. robini (trnR, trnM, trnY, trnS 1 , trnA) could only be identified manually by sequence alignment and secondary structure comparison with those identified in other species of sarcoptiform mites [8, 15, 18, 20,21,22,23,24,25, 28]. The putative mt tRNA genes were highly truncated in both H. feroniarum (48 to 61 bp) and R. robini (47 to 63 bp) (Additional file 1: Figure S1), missing either D-arm or T-arm, except tRNA-Lys, which has the typical cloverleaf secondary structure in both mites. Further, the putative tRNA-Arg of R. robini does not have a D-arm, nor a T-arm. Most of the putative tRNA genes also have mismatches on T-arm, D-arm, acceptor arm or anticodon arm (Additional file 1: Figure S1).
Genes are on both strands of the mt genomes of R. robini and H. feroniarum. In R. robini, J-strand has 26 genes whereas the N-strand has 11 genes. In H. feroniarum, J-strand has 27 genes whereas the N-strand has 10 genes. The start codons of the 13 PCGs were ATN and the stop codons were TAA or TAG in both H. feroniarum (Additional file 3: Table S2) and R. robini (Additional file 2: Table S1). Incomplete stop codons, T, was found in protein-coding genes that precede a tRNA gene in R. robini. The two longest non-coding regions (NCRs) in H. feroniarum are 100 bp in size between rrnL and trnI and 143 bp between nad4 and trnH (Fig. 1). We annotated these two NCRs as the putative control regions (CR) of H. feroniarum. The putative CR of R. robini is 319 bp between trnF and trnS 1 . No conserved sequences were found between the CRs of the two sarcoptiform mites. No other NCRs longer than 100 bp were found in the mt genomes of these two mites.
Most of the mt genes are rearranged in R. robini and H. feroniarum relative to the inferred ancestral mt genome of arthropods (Fig. 1) [2, 29]. Currently five types of mt gene order were found in the 12 species the sarcoptiform mites, for which mt genomes have been sequenced (Fig. 1). R. robini has a common Type I gene order, which has been found in seven other species from different genera and families. H. feroniarum has a Type II gene order, which is only found in this species. Type III and Type V gene orders are also restricted to single species. Two Tyrophagus species have Type IV gene order (Fig. 1).
Retrieving the “lost” mt tRNA genes in sarcoptiform mites
We applied the manual tRNA gene search approach above to St. magnus, T. longior, T. putrescentiae and Sa. scabiei, which were reported to have lost 2 to 16 tRNA genes in their mt genomes [8, 15, 17, 18]. These “lost” tRNA genes cannot be identified by tRNAscan-SE nor ARWEN programs with all possible parameters we tested. In our manual approach, we focused on the gap regions (46–215 bp) between identified genes where the anticodon sequences of the “lost” tRNA genes can be identified. We then aligned the sequences of these gap regions with those of the candidate tRNA genes identified in other species of sarcoptiform mites, and compared the inferred secondary structure with each other (Fig. 2, 3 and Additional file 4: Figure S2). Based on the overall secondary structure, we retrieved the two “lost” tRNA genes, trnA and trnY, in Sa. scabiei (Fig. 4) and all of the 16 “lost” tRNA genes (trnC, trnG, trnK, trnT, trnY, trnA, trnD, trnR, trnS 1 , trnF, trnV, trnL 1 , trnM, trnN, trnE and trnI) in St. magnus (Fig. 5). The two “lost” tRNA genes, trnF and trnS 1 , were also retrieved in T. longior and T. putrescentiae (Fig. 4), whereas trnQ was not retrieved by our manual approach. Of the 16 tRNA genes of St. magnus retrieved manually, five tRNA genes (trnC, trnD, trnG, trnK and trnT) are more conserved in nucleotide sequence than the other 11 tRNA genes (trnA, trnE, trnF, trnI, trnL 1 , trnM, trnN, trnR, trnS 1 , trnV and trnY) when compared with those of other species of sarcoptiform mites (Figs. 2, 3 and 5). The secondary structure inferred from these manually retrieved tRNA gene sequences is either T-armless or D-armless, and has 1–2 mismatches on the AC-stem or 1–4 mismatches on AA-stem (Figs. 4 and 5). Apparently, the severe truncation and mismatches contribute to the failure of identifying these tRNA genes by tRNAscan-SE and ARWEN programs. Furthermore, less common anticodon sequences are seen in a number of tRNA genes that we identified manually: trnE (CUC instead of UUC) and trnI (AAU instead of GAU) of St. magnus (Fig. 5); trnC (ACA instead of GCA), trnI (AAU instead of GAU) and trnQ (CUG instead of UUG) of H. feroniarum (Fig. 4); trnF (AAA instead of GAA) and trnS 1 (ACU instead of GCU) of T. longior and T. putrescentiae (Fig. 4).
It is noteworthy that four “lost” tRNA genes of St. magnus, trnE, trnG, trnP and trnS 1 , were also retrieved by Edwards et al. ; two of these tRNA genes, trnG and trnS 1 , were at the same location as we inferred, but were different in the sequences of AA-stems. trnE was abnormally inferred within nad5 by Edwards et al. , whereas we retrieved trnE in a gap where no other genes were found. Clearly, the comparative approach we used has its limits. Further evidence is required to establish the exact locations of the “lost” tRNA genes of St. magnus, such as transcriptional data of its mt tRNA, and sequence comparison among closely related Steganacarus species.
Codon usage in the mt genomes of sarcoptiform mites
There is no evidence yet that nuclear tRNA genes can be imported into mitochondria in mites or other animals. If a mt tRNA gene is indeed lost and there is no nuclear replacement, then its corresponding codons in the mt protein-coding genes will not be translated. We analyzed the codon usage in the mt protein-coding genes of the 12 species of sarcoptiform mites to see whether or not, and how, the corresponding codons of the “lost” tRNA genes are used. Overall, the codon use is very similar across all sarcoptiform mites. The most frequently used codons are for amino acids Phe (11.2–15.3%), Leu (7.1–10.0%), Met (6.3–10.0%), Ser (7.4–9.5%), Val (4.4–8.8%) and Ile (6.1–10.6%) (Additional file 5: Table S3, Fig. 6, Additional file 6: Figure S3). The least used codons are for Gln (0.9–1.4%), Cys (1.0–2.1%), Arg (1.0–1.4%), His (1.5–1.8%) and Trp (1.9–2.8%) (Additional file 5: Table S3). Codons for all of the 22 amino acids are present in all of the protein-coding genes in all of the sarcoptiform mites, including the four species in which mt tRNA gene “loss” has been reported (Fig. 6). The frequency of each codon is also very similar across all of the sarcoptiform mites.
Mitochondria have their own transcription and translation systems, separate from the nuclear systems . The tRNA genes encoded by mt genomes are critical to the mt translation system. With few exceptions, animal mt genomes encode 22 tRNA genes for the 20 amino acids used in protein synthesis . Loss of any of the 22 mt tRNA genes will severely affect the translation system in mitochondria unless a nuclear equivalent can be imported into mitochondria. Loss of tRNA genes have been reported in the mt genomes of four species of sarcoptiform mites [8, 15, 17, 18]. However, convincing evidence for the loss of mt tRNA genes in these mites is lacking; alternative possibilities have not been explored. Here, we show that all of the “lost” tRNA genes except one (trnQ of T. putrescentiae) can be found by a manual comparative approach . Furthermore, our codon use analysis does not support the loss of any of the 22 mt tRNA genes in sarcoptiform mites because the overall codon usage is very similar across all sarcoptiform mites including those in which mt tRNA genes were reported as lost [8, 15, 17, 18].
Instead of loss, we propose that it is the highly unusual secondary structure of inferred mt tRNA genes that makes them unidentifiable by the tRNA search programs. The mt tRNA genes of animals usually possess a cloverleaf secondary structure with four arms: AA-arm, D-arm, AC-arm and T-arm . The only exception is the tRNA for serine (anticodon GCT), which lack a D-arm in nearly all animals; this is apparently an ancestral feature for animals . Using a manual comparative approach, we were able to identify all of the 16 “lost” tRNA genes in St. magnus, three in H. feroniarum, two of the three in T. longior and T. putrescentiae, and two in Sa. scabiei. These retrieved tRNA genes are either D-armless or T-armless and have many mismatches at AA-stems and AC-stems. Clearly, the highly unconventional structure prevented them from being found by the tRNA search programs.
Post-transcriptional tRNA editing is likely common and necessary in the mitochondria of sarcoptiform mites. Mt. tRNA editing has been reported in centipede , velvet worms  and sponges , where nucleotides can be substituted, inserted and/or deleted from transcripts. Mt. tRNA editing has largely been found at the 3′ end of the AA-stems in metazoan [33,34,35,36], also in rebuilding T-arm, variable loop or even AC-stem . Within the class Arachnida, mt tRNA editing was suggested to form AA-stems in spiders [37, 38]. Investigation into tRNA editing in sarcoptiform mites is apparently needed.
In summary, using a manual comparative approach, we were able to identify all of the mt tRNA genes which were reported previously as lost in sarcoptiform mites except for trnQ of T. putrescentiae. Our codon usage analysis does not support the loss of any mt tRNA genes in sarcoptiform mites. Instead, the mt tRNA genes reported as “lost” previously in sarcoptiform mites have unusual secondary structures and contain many nucleotide mismatches. Post transcriptional tRNA editing is likely common and necessary in sarcoptiform mites and need to be investigated in future studies.
Collection of mites
H. feroniarum and R. robini were collected from mushrooms (Pleurotus ostreatus) in March 2015 at the Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, China. Mite samples were either used immediately for DNA extraction or were preserved in 100% ethanol at − 20 °C prior to DNA extraction. Samples of each mite species were also mounted to slides as voucher, using Hoyer’s medium for morphological check with Zeiss A2 (microphoto camera AxioCam MRc) microscope. All of the specimens and vouchers were deposited at the Arthropod Collection, Department of Entomology, Nanjing Agricultural University, China.
DNA extraction, mt genome amplification and sequencing
Genomic DNA was extracted from individuals, using a DNeasy Blood and Tissue Kit (QIAGEN), following the modified protocol . For H. feroniarum, a 658-bp fragment of cox1 was initially amplified by PCR with the primer pairs LCO1490–HCO2198  (Additional file 7: Table S4). PCR products were purified and sequenced directly using the Sanger method at Majorbio (Shanghai, China). Specific primers for H. feroniarum, HCOIF1 and HCOIR1, were designed from the sequences of the cox1 fragment. PCR with these two primers produced a 13.5-kb amplicon, which was sequenced with Illumina Hiseq 2000 platform at the Majorbio (Shanghai, China).
For R. robini, a 395-bp fragment of cob and a 357-bp fragment of rrnS were initially amplified by PCR with the primer pairs CytbF–CytbR  and SR-J-14199–SR-J-14199  (see Additional file 7: Table S4). The PCR products were purified and sequenced directly using Sanger method at Majorbio. Two pairs of specific primers, R412SF1–R4COBR1 and R4COBF2–R412SR3, were designed from the sequences of the cob and rrnS fragments. The PCR with R412SF1–R4COBR1 produced a 5.8-kb amplicon. The PCR with R4COBF2–R412SR3 produced an 8.4-kb amplicon. Both amplicons were sequenced with Illumina Hiseq 2000 platform at the Majorbio.
The initial PCRs contained 12.5 μL of PCR SuperMix (Transgene Biotech Co., Ltd., Beijing, China), 2 μl of template DNA, and 1.25 μM of each primer, for a total volume of 25 μL. The PCR cycling conditions were: 3-min denaturation at 96 °C; 35 cycles of 10-s denaturation at 95 °C, 30-s annealing at 46 °C and 1.5-min extension at 72 °C; 5-min final extension at 72 °C. Then, the PCRs were held at 4 °C. PCR products were checked on 1% agarose gel. PrimeSTAR GXL DNA polymerase (TAKARA) was used in the long PCRs with the cycling conditions: 35 cycles of 98 °C for 10 s, 68 °C for 5 to 10 min (depends on the length of regions between rrnS and cob). The reaction mixture contained 0.5 μl GXL DNA Polymerase, 5 μl buffer, 2 μl dNTP mixture, 0.75 μl of each primer, 1 μl of template DNA and Milli-Q water added to a total volume of 25 μl. Positive and negative controls were executed with each PCR. PCR products were checked on 1% agarose gel. PCR products were purified with QIAquick Spin PCR Purification Kit (QIAGEN).
Assembly of Illumina sequence-reads, gene identification and codon usage analysis
Illumina sequence-reads obtained from the mt genome amplicons of H. feroniarum and R. robini were assembled into contigs with Geneious 8.1.2 (Biomatters Ltd.). The tRNA genes were identified using tRNAscan-SE  and ARWEN  or identified manually based on anticodons and secondary structures. tRNA genes of the two sarcoptiform mites were verified by comparison of secondary structures and conserved nucleotide sequences with those of the Acari species reported in published literature. PCGs were identified by open reading frame search in Geneious and BLAST searches of GenBank . The two rRNA genes, rrnL and rrnS, were also identified by BLAST searches of GenBank based on sequence similarity and conserved sequence motifs. The start and stop nucleotides of rrnL and rrnS cannot be determined exactly and were assumed to be immediately after their upstream genes and before their downstream genes. The nucleotide sequences of mt genomes of H. feroniarum and R. robini have been deposited in GenBank under accession numbers MF596167 and MF596168. The codon usage and Relative Synonymous Codon Usage (RSCU) values were analyzed with MEGA 6.0.6 .
Retrieving the “lost” mt tRNA genes in sarcoptiform mites
Mitochondrial genome sequences of T. longior, T. putrescentiae, Sa. scabiei and St. magnus were retrieved from NCBI (Additional file 8: Table S5). We surveyed the “lost” tRNA genes using tRNAscan-SE  and ARWEN  and then manually identified the “lost” tRNA genes. We focused on the gap regions (46–215 bp) between identified genes where the anticodon sequences of the “lost” tRNA genes could be found. To find conserved nucleotides in anticodon loops, the nucleotide sequences of 17 “lost” tRNA genes (trnA, trnC, trnD, trnE, trnF, trnG, trnI, trnK, trnL 1 , trnM, trnN, trnQ, trnR, trnS 1 , trnT, trnV and trnY) of sarcoptiform mites were aligned using MUSCLE algorithm in Geneious 8.1.2. and manually formed the secondary structures. The nucleotide sequences of anticodon loops are relatively conserved in these sarcoptiform mites (Figs. 2, 3 and Additional file 4: Figure S2).
To get more species of oribatid mites for comparison with Steganacarus magnus, we also retrieved and analyzed the whole genome sequence data of three oribatid mites available in NCBI, i.e., Platynothrus peltifer (ID: 37201), Hypochthonius rufulus (ID: 37200), Achipteria coleoptrata (ID: 37199) (Additional file 8: Table S5). We searched the mt genome sequences and contigs of these oribatid mites from their whole genome sequence data using the sequence of their cox1 as a reference. Unfortunately, the coverage of mt genomes is very low in the whole genome sequence data of these 3 oribatid mites. We found only mt trnK for Pl. peltifer from one contig (GenBank accession number LBFO01104924.1, Fig. 2) but no mt tRNA genes for Hypochthonius rufulus and Achipteria coleoptrata.
- atp6 and atp8 :
Genes for ATP synthase subunits 6 and 8
- cob :
Gene for cytochrome b
- cox1, cox2 and cox3 :
Genes for cytochrome c oxidase subunits 1, 2 and 3
Kilo base pair
- nad1, nad2, nad3, nad4, nad4L, nad5 and nad6 :
Mitochondrial genes for NADH dehydrogenase subunits 1–6 and 4 L
Polymerase chain reaction
- rrnS and rrnL :
Genes for small and large subunits of ribosomal RNA
Relative Synonymous Codon Usage
- trnA or A:
tRNA gene for alanine
- trnC or C:
tRNA gene for cysteine
- trnD or D:
tRNA gene for aspartic acid
- trnE or E:
tRNA gene for glutamic acid
- trnF or F:
tRNA gene for phenylalanine
- trnG or G:
tRNA gene for glycine
- trnH or H:
tRNA gene for histidine
- trnI or I:
tRNA gene for isoleucine
- trnK or K:
tRNA gene for lysine
- trnL 1 or L1 :
tRNA gene for leucine (anticodon NAG)
- trnL 2 or L2 :
tRNA gene for leucine (anticodon YAA)
- trnM or M:
tRNA gene for methionine
- trnN or N:
tRNA gene for asparagine
- trnP or P:
tRNA gene for proline
- trnQ or Q:
tRNA gene for glutamine
- trnR or R:
tRNA gene for arginine
- trnS 1 or S1 :
tRNA gene for serine (anticodon NCU)
- trnS 2 or S2 :
tRNA gene for serine (anticodon NGA)
- trnT or T:
tRNA gene for threonine
- trnV or V:
tRNA gene for valine
- trnW or W:
tRNA gene for tryptophan
- trnY or Y:
tRNA gene for tyrosine
Lane N. Power, sex, suicide: mitochondria and the meaning of life. New York: Oxford University Press; 2006.
Boore JL. Animal mitochondrial genomes. Nucleic Acids Res. 1999;27:1767–80.
Okimoto R, Chamberlin HM, Macfarlane JL, Wolstenholme DR. Repeated sequence sets in mitochondrial DNA molecules of root knot nematodes (Meloidogyne): nucleotide sequences, genome location and potential for host-race identification. Nucleic Acids Res. 1991;19:1619–26.
Hoffmann RJ, Boore JL. Brown WM. A novel mitochondrial genome organization for the blue mussel, Mytilus edulis. Genetics. 1992;131:397–412.
Beagley CT, Okada NA, Wolstenholme DR. Two mitochondrial group I introns in a metazoan, the sea anemone Metridium senile: one intron contains genes for subunits 1 and 3 of NADH dehydrogenase. Proc Natl Acad Sci U S A. 1996;93:5619–23.
Le TH, Blair D, McManus DP. Mitochondrial genomes of parasitic flatworms. Trends Parasitol. 2002;18:206–13.
Dávila S, Piñero D, Bustos P, Cevallos MA, Dávila G. The mitochondrial genome sequence of the scorpion Centruroides limpidus (Karsch 1879) (Chelicerata; Arachnida). Gene. 2005;360:92–102.
Domes K, Maraun M, Scheu S, Cameron SL. The complete mitochondrial genome of the sexual oribatid mite Steganacarus magnus: genome rearrangements and loss of tRNAs. BMC Genomics. 2008;9:532. https://doi.org/10.1186/1471-2164-9-532.
Jeyaprakash A, Hoy MA. The mitochondrial genome of the predatory mite Metaseiulus occidentalis (Arthropoda: Chelicerata: Acari: Phytoseiidae) is unexpectedly large and contains several novel features. Gene. 2007;391:264–74.
Zhang Z-Q. Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa. 2011;3148:7–12.
Krantz G, Walter D. A manual of acarology. third ed. Lubbock: Tech University Press; 2009.
Zhang Z-Q. Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Auckland: Magnolia Press; 2011.
Lloyd CM. Dust mites’ dirty dealings in the lung. Nat Med. 2009;15:366–7.
Hammad H, Chieppa M, Perros F, Willart MA, Germain RN, Lambrecht BN. House dust mite allergen induces asthma via toll-like receptor 4 triggering of airway structural cells. Nat Med. 2009;15:410–6.
Mofiz E, Seemann T, Bahlo M, Holt D, Currie BJ, Fischer K, Papenfuss AT. Mitochondrial genome sequence of the ccabies mite provides insight into the genetic diversity of individual scabies infections. PLoS Negl Trop Dis. 2016;10(2):e0004384. https://doi.org/10.1371/journal.pntd.0004384.
Palyvos NE, Emmanouel NG, Saitanis CJ. Mites associated with stored products in Greece. Exp Appl Acarol. 2008;44:213–26.
Que S, Zou Z, Xin T, Xia B. Complete mitochondrial genome of the mold mite, Tyrophagus putrescentiae (Acari: acaridae). Mitochondrial DNA. 2014;27:688–9.
Yang B, Li C. Characterization of the complete mitochondrial genome of the storage mite pest Tyrophagus longior (Gervais) (Acari: acaridae) and comparative mitogenomic analysis of four acarid mites. Gene. 2016;576:807–19.
Edwards DD, Jackson LE, Johnson AJ, Ernsting BR. Mitochondrial genome sequence of Unionicola parkeri (Acari: Trombidiformes: Unionicolidae): molecular synapomorphies between closely-related Unionicola gill mites. Exp Appl Acarol. 2011;54:105–17.
Sun ET, Li CP, Nie LW, Jiang YX. The complete mitochondrial genome of the brown leg mite, Aleuroglyphus ovatus (Acari: Sarcoptiformes): evaluation of largest non-coding region and unique tRNAs. Exp Appl Acarol. 2014;64:141–57.
Sun E, Li C, Li S, Gu S, Nie L. Complete mitochondrial genome of Caloglyphus berlesei (acaridae: Astigmata): the first representative of the genus Caloglyphus. J Stored Prod Res. 2014;59:282–4.
Klimov PB, Oconnor BM. Improved tRNA prediction in the American house dust mite reveals widespread occurrence of extremely short minimal tRNAs in acariform mites. BMC Genomics. 2009;10:598. https://doi.org/10.1186/1471-2164-10-598.
Dermauw W, Van Leeuwen T, Vanholme B, Tirry L. The complete mitochondrial genome of the house dust mite Dermatophagoides pteronyssinus (Trouessart): a novel gene arrangement among arthropods. BMC Genomics. 2009;10:107. https://doi.org/10.1186/1471-2164-10-107.
Lee C-C, Wang J. The complete mitochondrial genome of Histiostoma blomquisti (Acari: Histiostomatidae). Mitochondrial DNA Part B. 2016;1:671–3.
Gu XB, Liu GH, Song HQ, Liu TY, Yang GY, Zhu XQ. The complete mitochondrial genome of the scab mite Psoroptes cuniculi (Arthropoda: Arachnida) provides insights into Acari phylogeny. Parasit Vectors. 2014;7:340. https://doi.org/10.1186/1756-3305-7-340.
Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res. 2005;33:W686–9.
Laslett D, Canback B. ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics. 2008;24:172–5.
Que S, Xin T, Yi J, Zou Z, Li L, Xia B. Complete mitochondrial genome of Aleuroglyphus ovatus (Acari: acaridae). Mitochondrial DNA. 2016;27:563–4.
Staton JL, Daehler LL, Brown WM. Mitochondrial gene arrangement of the horseshoe crab Limulus polyphemus L.: conservation of major features among arthropod classes. Mol Biol Evol. 1997;14:867–74.
Barrell BG, Anderson S, Bankier A, de Bruijn M, Chen E, Coulson A, Drouin J, Eperon I, Nierlich D, Roe B. Different pattern of codon recognition by mammalian mitochondrial tRNAs. Proc Natl Acad Sci U S A. 1980;77:3164–6.
Xue XF, Guo JF, Dong Y, Hong XY, Shao R. Mitochondrial genome evolution and tRNA truncation in Acariformes mites: new evidence from eriophyoid mites. Sci Rep. 2016;6:18920. https://doi.org/10.1038/srep18920.
Wolstenholme DR. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 1992;141:173–216.
Lavrov DV, Brown WM, Boore JL. A novel type of RNA editing occurs in the mitochondrial tRNAs of the centipede Lithobius forficatus. Proc Natl Acad Sci U S A. 2000;97:13738–42.
Segovia R, Pett W, Trewick S, Lavrov DV. Extensive and evolutionarily persistent mitochondrial tRNA editing in velvet worms (phylum Onychophora). Mol Biol Evol. 2011;28:2873–81.
Lavrov DV, Pett W, Voigt O, Wörheide G, Forget L, Lang BF, Kayal E. Mitochondrial DNA of Clathrina clathrus (Calcarea, Calcinea): six linear chromosomes, fragmented rRNAs, tRNA editing, and a novel genetic code. Mol Biol Evol. 2013;30:865–80.
Börner GV, S-i Y, Mörl M, Dörner M, Pääbo S. RNA editing in metazoan mitochondria: staying fit without sex. FEBS Lett. 1997;409:320–4.
Masta SE, Boore JL. The complete mitochondrial genome sequence of the spider Habronattus oregonensis reveals rearranged and extremely truncated tRNAs. Mol Biol Evol. 2004;21:893–902.
Masta SE, Boore JL. Parallel evolution of truncated transfer RNA genes in arachnid mitochondrial genomes. Mol Biol Evol. 2008;25:949–59.
Dabert J, Ehrnsberger R, Dabert M. Glaucalges tytonis sp. n. (Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigiformes, Tytonidae): compiling morphology with DNA barcode data for taxon descriptions in mites (Acari). Zootaxa. 2008;1719:41–52.
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294–9.
Boore JL, Brown WM. Mitochondrial genomes of Galathealinum, Helobdella, and Platynereis: sequence and gene arrangement comparisons indicate that Pogonophora is not a phylum and Annelida and Arthropoda are not sister taxa. Mol Biol Evol. 2000;17:87–106.
Kambhampati S, Smith PT. PCR primers for the amplification of four insect mitochondrial gene fragments. Insect Mol Biol. 1995;4:233–6.
Benson DA, Cavanaugh M, Clark K, Karsch-Mizrachi I, Lipman DJ, Ostell J, Sayers EW. GenBank. Nucleic Acids Res. 2013;41:D36–42.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 2013;30:2725–9.
We thank Dr. Enrico Negrisolo (University of Padova, Italy) for his valuable comments on this manuscript. We also thank two anonymous reviewers for comments that have greatly improved this manuscript.
This research was funded by the National Natural Science Foundation of China (31672337), the Fundamental Research Funds for the Central Universities (KYZ201405), the Australian Research Council (DP120100240 to RS) and Australia-China Science & Research Fund (ACSRF00980 to RS).
Availability of data and materials
The mt genomes of Histiostoma feroniarum and Rhizoglyphus robini are available on GenBank under the accession numbers MF596167 and MF596168. All supporting data are included as Additional files.
Ethics approval and consent to participate
No specific permits were required for the mites collected for this study in China. The mite specimens were collected from mushrooms, and the field studies did not involve endangered or protected species. The species in our study are common mites and are not included in the “List of Protected Animals in China”.
Consent for publication
The authors declare that they have no competing interests.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Figure S1. Inferred secondary structure of 19 mitochondrial tRNA genes of Histiostoma feroniarum (Hf) and 22 mitochondrial tRNA genes of Rhizoglyphus robini (Rr). tRNA genes are labeled with the abbreviations of their corresponding amino acids. Dashes indicate Watson–Crick bonds; dots indicate bonds between U and G. Shared identical sequences between tRNA genes are circled in H. feroniarum. (PDF 3430 kb)
Table S1. Mitochondrial genome organization of Rhizoglyphus robini. (DOCX 13 kb)
Table S2. Mitochondrial genome organization of Histiostoma feroniarum. (DOCX 16 kb)
Figure S2. The alignment of nucleotide sequences of nine mitochondrial putative tRNA genes (encoded by trnA, trnE, trnF, trnI, trnQ, trnR, trnS 1 , trnV and trnY) in the Sarcoptiformes mites. The conserved sequences in anticodon loops were marked. (PDF 4582 kb)
Table S3. Amino acid frequencies of the sarcoptiform mites. (DOCX 16 kb)
Figure S3. Relative synonymous codon usage (RSCU) and codon numbers for five amino acids (H, L2, P, S2 and W) in the mitochondrial genomes of sarcoptiform mites. The X-axis shows the sarcoptiform mites, and the Y-axis shows the RSCU or total number of codons. The blue column indicates the codons that match the anticodons of the corresponding mt tRNA genes. The red, green and purple column indicate the imperfect, synonymous codons to the anticodons of their corresponding mt tRNA genes. (PDF 635 kb)
Table S4. PCR primers used in this study. (DOCX 13 kb)
Table S5. Sarcoptiform mites included in this study. (DOCX 18 kb)
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Xue, XF., Deng, W., Qu, SX. et al. The mitochondrial genomes of sarcoptiform mites: are any transfer RNA genes really lost?. BMC Genomics 19, 466 (2018). https://doi.org/10.1186/s12864-018-4868-6
- Mitochondrial genome
- tRNA structure
- Histiostoma feroniarum
- Rhizoglyphus robini