Research Article |
Corresponding author: Andrzej Lesicki ( alesicki@amu.edu.pl ) Academic editor: Thierry Backeljau
© 2022 Ewa Kosicka, Joanna R. Pieńkowska, Andrzej Lesicki.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kosicka E, Pieńkowska JR, Lesicki A (2022) The complete mitochondrial genome of the terrestrial snail Monacha cartusiana (O.F. Müller, 1774) (Gastropoda, Eupulmonata, Hygromiidae). ZooKeys 1130: 65-78. https://doi.org/10.3897/zookeys.1130.91325
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The mitochondrial genome of Monacha cartusiana is the first complete mitochondrial sequence described for the pulmonate snail genus Monacha and for the family Hygromiidae. The identified mitogenome has a length of 13,894 bp and encodes 13 proteins, 22 tRNAs, and two rRNAs. A phylogenetic analysis of available mitogenomes from representatives of helicoid families shows a sister group relationship of Hygromiidae and Geomitridae, which have been recently recognised as separate families.
Carthusian snail, Helicoidea, mitogenome, phylogeny, Stylommatophora
Mollusca is the second largest animal phylum after Arthropoda in terms of the number of named species, with the class Gastropoda as the most speciose group with approximately 95,000 species (
Mitogenome sequences are of great importance in molecular phylogenetic studies (
The hygromiid genus Monacha Fitzinger, 1833 is widespread in the western Palaearctic from western Europe to North Africa, Iran, and Arabia. It includes a large number of nominal species and shows its highest diversity in south-eastern Europe and Turkey (
The specimen of Monacha cartusiana used for this research was collected in Ostrowiec Świętokrzyski (Poland) by Mariusz Gwardjan on 03.07.2015. It was identified by the sequence of the cytochrome c oxidase subunit I gene fragment (coI) of M. cartusiana in GenBank (KX258398) deposited by
List of primers used for the amplification of Monacha cartusiana mitochondrial DNA.
Primer | Sequence 5' – 3' | References |
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LCO1490 | GGTCAACAAATCATAAAGATATTGG |
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HC02198 | TAAACTTCAGGGTGACCAAAAAATCA |
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16Sar-L | CGCCTGTTTATCAAAAACAT |
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16Sbr-H | CCGGTCTGAACTCAGATCACGT |
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144F | TGAGSNCARATGTCNTWYTG |
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272R | GCRAANAGRAARTACCAYTC |
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FCOII | AAATAATGCTATTTCATGAYCAYG |
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RCOII | GCTCCGCAAATCTCTGARCAYTG |
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1F_556 Os | TACCTGTACTAGCGGGGGCT | this paper |
1R_75 Os | CAGTCAGGGTACTGCGGCTA | this paper |
2F_342 Os | TTGTGACCTCGATGTTGGACT | this paper |
2R_83 Os | CCGCCTCAGACCCAACTAAC | this paper |
3F_320 Os | GGCCTAACTTGTTCACTGATCCT | this paper |
3R_50 Os | TTTCTAGGGTCTGCGCTTCA | this paper |
4F_429 Os | TTGTGGGGGTTTATTACGGGC | this paper |
4R_110 Os | ATCACTCAACACCCCTGAAGT | this paper |
seqF_F1 | ACGGTTTCCTGTTCTATTATTTG | this paper |
seqF_R1 | CAAATAATAAGCTCCTAATGTAATC | this paper |
seqF_R2 | ATAAACTTTCCACTTCAGGGAAT | this paper |
seqF_R3 | GTAAAACATTTATTGGGGCCCAG | this paper |
seqF_R4 | AACTAATTAACAACCTATATAGGG | this paper |
seqF_R5 | TAGTCCCGTGCTGGCTAGTATT | this paper |
seqH_F2 | CTATTGTAACTCGCCTTAACTCTAA | this paper |
seqH_R2 | GAAATAAACACCTAAAATTACTGTA | this paper |
seqH_R3 | GATGTACCTGATATTAAACCTA | this paper |
seqH_F4 | CTACTAAACAGAAAAAGCGAACCC | this paper |
seqH_R4 | GCAGCCACAATTTACTTCTT | this paper |
The mitogenome was annotated using the MITOS Web Server (
Mitogenomes from GenBank used in the phylogenetic analysis and their lengths.
species | GenBank Accession No. | Mitogenome length (bp) | References |
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Camaenidae: Aegista aubryana (Heude, 1882) | KT192071 | 14238 |
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Camaenidae: Aegista diversifamilia Huang, Lee, Lin & Wu, 2014 | KR002567 | 14039 |
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Camaenidae: Camaena cicatricosa (O. F. Müller, 1774) | KM365408 | 13843 |
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Camaenidae: Camaena poyuensis Zhou, Wang & Ding, 2016 | KT001074 | 13798 |
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Camaenidae: Dolicheulota formosensis (Adams, 1866) | KR338956 | 14237 |
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Camaenidae: Fruticicola koreana (L. Pfeiffer, 1850) | KU237291 | 13979 |
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Camaenidae: Mastigeulota kiangsinensis (Martens, 1875) | KM083123 | 14029 |
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Geomitridae: Cernuella virgata (Da Costa, 1778) | KR736333 | 14147 |
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Geomitridae: Helicella itala (Linnaeus, 1758) | KT696546 | 13967 |
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Helicidae: Cylindrus obtusus (Draparnaud, 1805) | JN107636 | 14610 |
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Helicidae: Cepaea nemoralis (Linnaeus, 1758) | U23045 | 14100 |
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Helicidae: Cornu aspersum (O. F. Müller, 1774) | JQ417194 | 14050 |
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Helicidae: Helix pomatia Linnaeus, 1758 | MK347426 | 14070 | Korabek et al. 2019 |
Helicidae: Helix pomatia Linnaeus, 1758 | MK488030 | 14072 |
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Helicidae: Helix pomatia Linnaeus, 1758 | MK488031 | 14070 |
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Helicidae: Theba pisana (O. F. Müller, 1774) | MH362760 | 14795 |
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Hygromiidae: Monacha cartusiana (O. F. Müller, 1774) | MW485067 | 13894 | This paper |
Polygyridae: Practicolella mexicana Perez, 2011 1 | KX278421 | 14008 |
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Polygyridae: Practicolella mexicana Perez, 2011 2 | KX240084 | 14153 |
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Arionidae: Arion vulgaris Moquin-Tandon, 1855 | MN607980 | 14548 |
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Philomycidae: Meghimatium bilineatum (Benson, 1842) | MG722906 | 14347 |
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Type | Gene product | Gene acronym | Start | End | Length (bp) | Direction | Start codon | Stop codon |
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PCG | cytochrome c oxidase subunit I | coI | 0 | 1552 | 1552 | + | ATG | TAA1 |
tRNA | valine transfer RNA | tRNA Val | 1525 | 1585 | 61 | + | ||
rRNA | 16S ribosomal RNA | 16S rRNA | 1242 | 2652 | 1410 | + | ||
tRNA | leucine transfer RNA | tRNA Leu | 2593 | 2657 | 65 | + | ||
tRNA | proline transfer RNA | tRNA Pro | 2654 | 2718 | 60 | + | ||
tRNA | alanine transfer RNA | tRNA Ala | 2716 | 2778 | 63 | + | ||
PCG | NADH dehydrogenase subunit 6 | nd6 | 2777 | 3263 | 451 | + | ATT | TAA |
PCG | NADH dehydrogenase subunit 5 | nd5 | 3316 | 4915 | 1657 | + | ATA | TAG |
PCG | NADH dehydrogenase subunit 1 | nd1 | 4896 | 5799 | 901 | + | ATA | TAA1 |
PCG | NADH dehydrogenase subunit 4L | nd4l | 5843 | 6076 | 233 | + | TTG | TAT |
PCG | cytochrome b | cytb | 6054 | 7192 | 1097 | + | GTC | TAA1 |
tRNA | aspartic acid transfer RNA | tRNA Asp | 7192 | 7263 | 71 | + | ||
tRNA | cysteine transfer RNA | tRNA Cys | 7250 | 7310 | 61 | + | ||
tRNA | phenylalanine transfer RNA | tRNA Phe | 7310 | 7369 | 60 | + | ||
PCG | cytochrome c oxidase subunit II | coII | 7370 | 8052 | 672 | + | ATG | TAA1 |
tRNA | tyrosine transfer RNA | tRNA Tyr | 8040 | 8102 | 55 | + | ||
tRNA | tryptophan transfer RNA | tRNA Trp | 8094 | 8158 | 65 | + | ||
tRNA | glycine transfer RNA | tRNA Gly | 8158 | 8223 | 66 | + | ||
tRNA | histidine transfer RNA | tRNA His | 8216 | 8274 | 58 | + | ||
tRNA | glutamine transfer RNA | tRNA Gln | 8274 | 8331 | 57 | - | ||
tRNA | leucine transfer RNA | tRNA Leu | 8320 | 8392 | 73 | - | ||
PCG | ATP synthase F0 subunit 8 | atp8 | 8385 | 8544 | 104 | - | ATG | TAA1 |
tRNA | asparagine transfer RNA | tRNA Asn | 8544 | 8602 | 59 | - | ||
PCG | ATP synthase F0 subunit 6 | atp6 | 8582 | 9242 | 661 | - | ATG | TAA |
tRNA | arginine transfer RNA | tRNA Arg | 9241 | 9304 | 62 | - | ||
tRNA | glutamic acid transfer RNA | tRNA Glu | 9303 | 9367 | 65 | - | ||
rRNA | 12S ribosomal RNA | 12S rRNA | 9412 | 10120 | 798 | - | ||
tRNA | metionine transfer RNA | tRNA Met | 10118 | 10180 | 63 | - | ||
PCG | NADH dehydrogenase subunit 3 | nd3 | 10160 | 10493 | 307 | - | ATT | TAA1 |
tRNA | serine transfer RNA | tRNA Ser | 10523 | 10576 | 53 | - | ||
tRNA | serine transfer RNA | tRNA Ser | 10648 | 10700 | 52 | + | ||
PCG | NADH dehydrogenase subunit 4 | nd4 | 10721 | 12005 | 1210 | + | ATT | TAG |
tRNA | threonine transfer RNA | tRNA Thr | 11996 | 12058 | 63 | - | ||
PCG | cytochrome c oxidase subunit III | coIII | 12046 | 12833 | 776 | - | ATG | TAA1 |
tRNA | isoleucine transfer RNA | tRNA Ile | 12877 | 12937 | 61 | + | ||
PCG | NADH dehydrogenase subunit 2 | nd2 | 12899 | 13872 | 833 | + | ATA | TAA1 |
tRNA | lysine transfer RNA | tRNA Lys | 13842 | 13894 | 60 | + |
Phylogenetic analysis was performed using maximum likelihood (ML) as implemented in the online version of IQ-TREE (
The complete mitogenome of M. cartusiana was deposited in GenBank under accession number MW485067. With 13,894 bp in length, it was one of the shortest mitogenomes known in Helicoidea, which ranged from 13,798 bp (Camaena poyuensis) to 14,795 bp (Theba pisana) (Table
Circular diagram of the mitochondrial genome of Monacha cartusiana (GenBank acc. no. MW485067). Genes encoded in the “plus” and the “minus” directions are shown outside and inside the circle, respectively. Particular gene types are marked with different colours: red – PCGs coding I, II, and III subunits of cytochrome c oxidase; green – PCGs coding NADH dehydrogenase family; orange – PCGs coding ATPase family; yellow – sequence coding cytochrome b; purple – tRNAs coding sequences; blue – rRNA coding genes. Noncoding sequences are mapped on a small inner circle. The circular diagram was created with GenomeVx (
Start and stop codons in the mitogenome protein coding genes of helicoid species.
Species | Start codons | Stop codons |
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Monacha cartusiana | ATA – 3; ATG – 5; ATT – 3; GTC – 1; TTG – 1 | TAA – 10; TAG – 2; TAT – 1 |
Cernuella virgata | ATA – 4; ATG – 4; ATT – 5 | TAA – 9; TAG – 4 |
Helix pomatia | ATA – 1; ATC – 1; ATG – 6; GTG – 3; TTG – 2 | TAA – 8; TAG – 5 |
Cepaea nemoralis | ATA – 5; ATG – 2; ATT – 6 | TAA – 2; TAG – 4; TA – 7 |
Cornu aspersum | ATA – 5; ATG – 6; TTG – 2 | TAA – 5; TAG – 5; T – 3 |
Theba pisana | ATA – 2; ATC – 1; ATG – 2; ATT – 8 | TAA/TAG – 12; T – 1 |
Cylindrus obtusus | ATA – 5; ATG – 4; ATC – 1; GTG – 1; TTG – 2 | TAA – 4; TAG – 5; T – 4 |
Practicolella mexicana | ATC – 1; ATG – 5; ATT – 2; GTG – 2; TTG – 3 | TAA – 3, TAG – 4; T – 6 |
Aegista aubryana | ATA – 6; ATG – 7 | TAA/TAG – 11; T – 2 |
Aegista diversifamilia | ATG – 5; ATT – 3; TTG – 3; TTA – 2 | TAA – 5; TAG – 2; TA – 2; T – 4 |
Camaena cicatricosa | ATA – 5; ATG – 4; ATT – 3; GTG – 1 | TAA – 11; TAG – 2 |
Dolicheulota formosensis | ATG – 4; ATA – 3; ATT – 3; TTG – 2; GTG – 1 | TAA – 5; TAG – 2; TA – 6 |
Mastigeulota kiangsinensis | ATA – 4; ATG – 7; ATT – 1; GTG – 1 | TAA – 7; TAG – 6 |
M. cartusiana | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
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C. virgata | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
H. itala | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
P. mexicana | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
H. pomatia | coI | Val | 16S | Leu | Ala | nd6 | Pro | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Thr | coIII | Ser | nd4 | Ile | nd2 | Lys | |
C. aspersum | coI | Val | 16S | Leu | Ala | nd6 | Pro | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Thr | coIII | Ser | nd4 | Ile | nd2 | Lys | |
C. nemoralis | coI | Val | 16S | Leu | Ala | nd6 | Pro | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Thr | coIII | Ser | nd4 | Ile | nd2 | Lys | |
C. obtusus | coI | Val | 16S | Leu | Ala | nd6 | Pro | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Tyr | Trp | Gly | His | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Thr | coIII | Ser | nd4 | Ile | nd2 | Lys | |
Ae. aubryana | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | nd3 | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
Ae. diversifamilia | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | nd3 | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
D. formosensis | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
F. koreana | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
M. kiangsinensis | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Asp | Cys | Phe | coII | Gly | His | Tyr | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
C. cicatricosa | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Cys | Phe | coII | Asp | Tyr | Gly | His | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys | |
C. poyuensis | coI | Val | 16S | Leu | Pro | Ala | nd6 | nd5 | nd1 | nd4l | cytb | Cys | Phe | coII | Asp | Tyr | Gly | His | Trp | Gln | Leu | atp8 | Asn | atp6 | Arg | Glu | 12S | Met | nd3 | Ser | Ser | nd4 | Thr | coIII | Ile | nd2 | Lys |
Phylogenetic analyses of the stylommatophoran mitogenomes (
For the phylogenetic analysis, a concatenated alignment of 12 PCGs (excluding atp8, because it was too short, too variable, and not annotated in the mitogenome of Cernuella virgata) and 2 rRNAs (12S and 16S) was used. The dataset included 19 helicoid species (Table
Maximum likelihood (ML) tree of mitochondrial genomes of species representing the superfamily Helicoidea (see Table
The mitogenome of M. cartusiana allows to add Hygromiidae to the previous analyses of Helicoidea families. It shows up in a clade with mitogenomes of the geomitrid species, Cernuella virgata and Helicella itala, confirming the close relationships of two families, i.e., Hygromiidae and Geomitridae (
We are grateful to Ondřej Korábek (Charles University, Prague, Czech Republic) and two anonymous reviewers for their constructive remarks, Thierry Backeljau (Royal Belgian Institute of Natural Sciences, Brussels, Belgium) for his editorial help, Robert A.D. Cameron (University of Sheffield, UK) for revising the English text, and Krzysztof Duda (Adam Mickiewicz University, Poznań) for help in preparing figures for print.