Complete Mitochondrial Genome and Novel Gene Organization of Ryssota otaheitana
(Pulmonata: Chronidae), and its Implications on the Stylommatophora Phylogeny
Amor M. Damatac II1* and Ian Kendrich C. Fontanilla1,2
1Institute of Biology, University of the Philippines,
Diliman, Quezon City 1101 Philippines
2Philippine Genome Center, University of the Philippines,
Diliman, Quezon City 1101 Philippines,
*Corresponding Author: This email address is being protected from spambots. You need JavaScript enabled to view it.
ABSTRACT
Whole mitochondrial genomes (mitogenomes) have been increasingly used as markers for phylogenetic inferences. In the Philippines, a marine snail from the Conidae family has been the only species to date whose mitogenome has been fully sequenced, despite the country’s rich malacofaunal diversity particularly in the terrestrial environment. In this study, we sequenced the complete mitogenome of the land snail Ryssota otaheitana (Chronidae), an endemic Philippine pulmonate species. The mitogenome is 13,888 bp in length and encodes the typical 37 genes – including 13 protein-coding, 22 tRNA, and 2 rRNA genes. Short intergenic spacers were found – including a reduced, 42-bp putative control region. Although the gene content is conserved, R. otaheitana showed a novel mitogenome organization involving the translocation of tRNASerine and NADH dehydrogenase subunit 4 gene segment. Combined with available stylommatophoran mitogenomes, different datasets from concatenated sequences of protein-coding and rRNA genes were used for phylogenetic reconstructions. Bayesian Inference (BI) and Maximum Likelihood (ML) trees congruently supported several monophyletic clades within the Stylommatophora such as the Helicoidea, Urocoptoidea, Orthurethra, and Limacoidea sensu lato (syn. ‘limacoid clade’). R. otaheitana is grouped with Deroceras reticulatum in the lower Stylommatophora and forms the monophyletic Limacoidea sensu lato. Both sequence-based phylogeny and gene order comparisons have led us to a hypothesis that Limacoidea sensu lato is at the base of the ‘non-achatinoid’ clade while supporting the division of ‘achatinoid and ‘non-achatinoid’ groups in the Stylommatophora. This study reports the first complete mitogenome from the Chronidae family, which can be used further for the molecular phylogeny of Philippine snails and gastropods at large.
INTRODUCTION
The suborder Stylommatophora comprises the majority of pulmonate gastropods and terrestrial mollusks in the world (Barker 2001). Its higher classification was traditionally based on the excretory system anatomy (Pilsbry 1900); however, groupings at the lower level were unclear due to inconsistent findings from morphological datasets (Shileyko 1979, Nordsieck 1986, Tillier, 1989). Given the challenges of traditional techniques, their lineage reconstructions have later shifted towards the use of molecular characters due to their higher resolving power. Wade et al. (2001) provided the first extensive molecular phylogeny of the Stylommatophora, which showed an unexpected separation into ‘achatinoid’ and ‘non-achatinoid’ groups. Such analyses have increased in the past years primarily due to the extent of molecular data to produce large sets of discrete, heritable, and unambiguous characters that can be effectively used for systematic inferences (Hillis 1987, Grauer and Li 2000). . . . . read more
REFERENCES
ABBOTT RT. 1989. Compendium of landshells: A color guide to more than 2,000 of the world’s terrestrial shells. USA: American Malacologists, p. 240.
AHN SJ, MARTIN R, RAO S, CHOI MY. 2017. The complete mitogenome of the gray garden slug Deroceras reticulatum (Gastropoda: Pulmonata: Stylommatophora). Mitochondr DNA Part B. 2: 255–256.
BARKER GM. 2001. Gastropods on land: phylogeny, diversity and adaptive morphology. In: The biology of terrestrial molluscs. Barker GM ed. United Kingdom: CABI Publishing. p. 1-139.
BERNT M, DONATH A, JÜHLING F, EXTERNBRINK F, FLORENTZ C, FRITZSCH G, PÜTZ J, MIDDENDORF M, STADLER PF. 2013. MITOS: Improved de novo metazoan mitogenome annotation. Mol Phylogenet Evol. 69: 313–319.
BOORE JL, BROWN WM. 1998. Big trees from little genomes: Mitochondrial gene order as a phylogenetic tool. Curr Opin Genet Dev. 8: 668–674.
BOORE JL. 1999. Animal mitogenomes. Nucleic Acid Res 27: 1767–1780.
BOORE JL, MACEY JR, MEDINA M. 2005. Sequencing and comparing whole mitogenomes of animals. Methods Enzymol. 395: 311–348.
BOORE JL. 2006. The complete sequence of the mitogenome of Nautilus macromphalus (Mollusca: Cephalopoda). BMC Genomics 7: 182.
BOSS KJ. 1971. Critical estimate of the number of Recent Mollusca. Occas Pap Mollusks. 3: 81–135.
BOUCHET P, ROCROI JP, FRÝDA J, HAUSDORF B, PONDER W, VALDÉS Á, WARÉN A. 2005. Classification and nomenclator of gastropod families. Malacologia 47(1–2).
CAMERON SL. 2014. Insect mitochondrial genomics: Implications for evolution and phylogeny. Annu Rev Entomol. 59: 95–117.
CASTRESANA J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540–552.
CHERNOMOR O, MINH BQ, VON HAESELER A. 2015. Consequences of common topological rearrangements for partition trees in phylogenomic inference. J Comput Biol 22: 1129–1142.
CUNHA RL, GRANDE C, ZARDOYA R. 2009. Neogastropod Phylogenetic Relationships based on Entire Mitogenomes. BMC Evol Biol 9: 210.
CUROLE J, KOCHER T. 1999. Mitogenomics: Digging deeper with complete mitogenomes. Trends Ecol Evol 14: 394–398.
DE CHAVEZ ERC, DE LARA AV. 2011. Diversity and spatial distribution patterns of macro land snails in Mount Makiling Forest Reserve, Philippines. Asia Life Sci 20: 183–197.
DOUBLET V, UBRIG E, ALIOUA A, BOUCHON D, MARCADÉ I, MARÉCHAL-DROUARD L. 2015. Large gene overlaps and tRNA processing in the compact mitogenome of the crustacean Armadillidium vulgare. RNA Biol 12: 1159–1168.
EGGER B, BACHMANN L, FROMM B. 2017. Atp8 is in the ground pattern of flatworm mitogenomes. BMC Genomics 18: 414.
FAUSTINO L. 1930. Summary of Philippine Land Shells. Philipp J Sci 48: 85–198.
FRANCINO MP, OCHMAN H. 1997. Strand asymmetries in DNA evolution. Trends in Genetics 13: 240–245.
GAITAN-ESPITIA JD, NESPOLO R, OPAZO JC. 2013. The Complete Mitogenome of the Land Snail Cornu aspersum (Helicidae: Mollusca): Intra-specific Divergence of Protein-Coding Genes and Phylogenetic Considerations within Euthyneura. PLoS ONE 8: e67299.
GISSI C, IANNELLI F, PESOLE G. 2008. Evolution of the mitogenome of Metazoa as exemplified by comparison of congeneric species. Heredity 101: 301.
GOTTING KJ. 1974. Malakozoologie: Grundriss der Weichtierkunde. Stuttgart: Gustav Fischer. p. 320.
GRANDE C, TEMPLADO J, ZARDOYA R. 2008. Evolution of gastropod mitogenome arrangements. BMC Evol Biol 8: 61.
GRAUER D, LI WH. 2000. Fundamentals of molecular evolution. Sunderland, MA: Sinauer Associates Inc.
GROENENBERG DSJ, HARL J, DUIJM E, GITTENBERGER E. 2017. The complete mitogenome of Orcula dolium (Draparnaud, 1801); Ultra-deep sequencing from a single long-range PCR using the Ion-Torrent PGM. Hereditas 154: 7.
HAUSDORF B. 1998. Phylogeny of the limacoidea sensu lato (gastropoda: stylommatophora). J Mollus Stud 64: 35–66.
HEANEY LR. 1986. Biogeography of mammals in SE Asia: Estimates of rates of colonization, extinction and speciation. Biol J Linn Soc 28: 127–165.
HEDTKE SM, TOWNSEND TM, HILLIS DM. 2006. Resolution of Phylogenetic Conflict in Large Data Sets by Increased taxon sampling. Syst Biol 55: 522–529.
HILLIS DM. 1987. Molecular versus morphological approaches to systematics. Ann Rev Ecol Syst 18: 23–42.
HOANG DT, CHERNOMOR O, VON HAESELER A, MINH BQ, VINH LS. 2017. UFBoot2: Improving the ultrafast bootstrap approximation. Molecular Biology and Evolution 35: 518–522.
LANFEAR R, CALCOTT B, HO SY, GUINDON S. 2012. PartitionFinder: Combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol Biol Evol 29: 1695–1701.
LANFEAR R, FRANDSEN PB, WRIGHT AM, SENFELD T, CALCOTT B. 2016. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34: 772–773.
LASLETT D, CANBÄCK B. 2008. ARWEN: A program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24: 172–175.
LOWE TM, EDDY SR. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25: 955–964.
LIU GH, WANG SY, HUANG WY, ZHAO GH, WEI SJ, SONG HQ, XU MJ, LIN RQ, ZHOU DH, ZHU XQ. 2012. The complete mitogenome of Galba pervia (Gastropoda: Mollusca), an intermediate host snail of Fasciola spp. PLoS ONE 7: e42172.
KLUSSMANN-KOLB A, DINAPOLI A, KUHN K, STREIT B, ALBRECHT C. 2008. From sea to land and beyond – New insights into the evolution of euthyneuran Gastropoda (Mollusca). BMC Evol Biol 8: 57.
KÜCK P, MEUSEMANN K. 2010. FASconCAT: convenient handling of data matrices. Mol Phylogenet Evol 56: 1115–1118.
MINTON RL, CRUZ MAM, FARMAN ML, PEREZ KE. 2016. Two complete mitogenomes from Praticolella mexicana Perez 2011 (Polygyridae) and gene order evolution in Helicoidea (Mollusca Gastropoda). Zookeys. 626: 137–154.
NABHAN AR, SARKAR IN. 2011. The impact of taxon sampling on phylogenetic inference: A review of two decades of controversy. Brief Bioinform 13: 122–134.
NGUYEN LT, SCHMIDT HA, VON HAESELER A, MINH BQ. 2014. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32: 268–274.
NORDSIECK H. 1986. The system of the Stylommatopohra (Gastropoda), with special regard to the systematic position of the Clausiliidae. In: II Importance of the Shell and distribution. Archiv für Molluskenkunde der Senckenbergischen Naturforschenden Gesellschaft 117: 93–116.
PILSBRY HA. 1900. On the Zoölogical Position of Partula and Achatinella. P Acad Nat Sci Phila 52: 561–567.
RAMBAUT A. 2018. FigTree v 1.4.4. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
RAWLINGS TA, MACINNIS MJ, BIELER R, BOORE JL, COLLINS TM. 2010. Sessile snails dynamic genomes: Gene rearrangements within the mitogenome of a family of caenogastropod molluscs. BMC Genomics 11: 440.
RAZKIN O, GÓMEZ-MOLINER BJ, PRIETO CE, MARTÍNEZ-ORTÍ A, ARRÉBOLA JR, MUÑOZ B, CHUECA LJ, MADEIRA MJ. 2015. Molecular phylogeny of the western Palaearctic Helicoidea (Gastropoda Stylommatophora). Mol Phylogenet Evol 83: 99–117.
ROKAS A, HOLLAND PWH. 2000. Rare genomic changes as a tool for phylogenetics. Trends Ecol Evol 15: 454–459.
RONQUIST F, HUELSENBECK JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.
SCHEFFERS BR, CORLETT RT, DIESMOS A, LAURANCE WF. 2012. Local demand drives a bushmeat industry in a Philippine forest preserve. Trop Conserv Sci 5: 133–141.
SHILEYKO AA. 1979. The system of the order Geophila (=Helicida) (Gastropoda: Pulmonata). Proc Zool Inst Acad Sci USSR 80: 44–69.
ŚMIETANKA B, BURZYŃSKI A, WENNE R. 2010. Comparative genomics of marine mussels (Mytilus spp.) gender associated mtDNA: Rapidly evolving atp8. J Mol Evol 71: 385–400.
SOLATRE JS. 2004. A promising component in agroforestry: Land snail called bayuku (Ryssota ovum). Asia-Pacific Agroforestry Newsletter 24: 7–8.
SOLEM A. 1978. Classification of the Land Mollusca. In: Pulmonates. Fretter V, Peake JF eds. London: Academic Press. p. 49–97.
SOSA III BOS, BATOMALAQUE GA, FONTANILLA IKC. 2014. An Updated Survey and Biodiversity Assessment of the Terrestrial Snail (Mollusca: Gastropoda) Species in Marinduque Philippines. Philipp J Sci 143: 199–210.
SPRINGSTEEN FJ, LEOBRERA FM. 1986. Shells of the Philippines. Philippines: Carfel Seashell Museum. 377p.
TILLIER S. 1989. Comparative morphology, phylogeny, and classification of land snails and slugs (Gastropoda: Pulmonata: Stylommatophora). Malacologia. 30: 1–303.
ULIANO-SILVA M, AMERICO JA, COSTA I, SCHOMAKER-BASTOS A, DE FREITAS REBELO M, PROSDOCIMI F. 2016. The complete mitogenome of the golden mussel Limnoperna fortunei and comparative mitogenomics of Mytilidae. Gene 577: 202–208.
WADE CM, MORDAN PB, CLARKE B. 2001. A phylogeny of the land snails (Gastropoda: Pulmonata). P Roy Soc Lond B Biol Sci 268: 413–422.
WADE CM, MORDAN PB, NAGSS F. 2006. Evolutionary relationships among the Pulmonate land snails and slugs (Pulmonata, Stylommatophora). Biol J Linn Soc 87: 593–610.
WANG P, YANG HF, HWANG CC, ZHANG WH, QIAN ZX. 2014. The mitogenome of the land snail Camaena cicatricosa (Müller 1774) (Stylommatophora Camaenidae): The first complete sequence in the family Camaenidae. Zookeys 451: 33–48.
WEIGERT A, GOLOMBEK A, GERTH M, SCHWARZ F, STRUCK TH, BLEIDORN C. 2016. Evolution of mitochondrial gene order in Annelida. Mol Phylogenet Evol 94: 196–206.
WHITE TR, CONRAD MM, TSENG R, BALAYAN S, GOLDING R, MARTINS AMDF, DAYRAT BA. 2011. Ten new complete mitogenomes of pulmonates (Mollusca: Gastropoda) and their impact on phylogenetic relationships. BMC Evol Biol 11: 295.
XIA X, XIE Z. 2001. DAMBE: software package for data analysis in molecular biology and evolution. J Hered 92: 371–373.
XIA X. 2012. DNA replication and strand asymmetry in prokaryotic and mitogenomes. Curr Genomics 13: 16–27.
YAMAZAKI N, UESHIMA R, TERRETT J, YOKOBORI S-L, KALFU M, SEGAWA R, KOBAYASHI T, NUMACHI K, UEDA T, NISHIKAWA K, WATANABE K, THOMAS RH. 1997. Evolution of pulmonate gastropod mitogenomes: Comparisons of gene organizations of Euhadra, Cepaea and Albinaria and implications of unusual tRNA secondary structures. Genetics 145: 749–758.
YANG T, XU G, GU B, SHI Y, MZUKA HL, SHEN H. 2019. The Complete Mitogenome Sequences of the Philomycus bilineatus (Stylommatophora: Philomycidae) and Phylogenetic Analysis. Genes 10: 198.
YOKOBORI S, PÄÄBO S. 1995. Transfer RNA editing in land snail mitochondria. Proc. Nat. Acad. Sci. USA 92: 10432–10435.
