Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 5277 No. 3: 3 May 2023
Type: Article
Published: 2023-05-03
DOI: 10.11646/zootaxa.5277.3.11
Page range: 585-599
Abstract views: 827
PDF downloaded: 250

Rediscovery of Bipalium admarginatum de Beauchamp, 1933 (Platyhelminthes, Tricladida, Geoplanidae) in Malaysia, with molecular characterisation including the mitogenome

Faculty of Applied Science; UCSI University; Kuala Lumpur; Malaysia
Institute of Marine and Environmental Sciences; University of Szczecin; Szczecin; Poland
30 Hurle Crescent; Bristol; BS8 2SZ; UK
James Cook University; Townsville; Queensland; Australia.
ISYEB; Institut de Systématique; Évolution; Biodiversité (UMR7205 CNRS; EPHE; MNHN; UPMC; Université des Antilles); Muséum National d’Histoire Naturelle; CP 51; 55 rue Buffon; 75231 Paris Cedex 05; France
Platyhelminthes Land flatworms 18S EF1-α mitochondrial genome phylogeny

Abstract

We present here the first observation of Bipalium admarginatum de Beauchamp, 1933 since its original description 90 years ago. Three specimens were found on Perhentian Kecil Island, off Terengganu State, Malaysia and photographed in the field, and two were collected. This report thus includes the first colour photographs published for this species, from a locality close to the type-locality, Tioman Island (which is ca. 200 km south of the locality in this study, on the east coast of Peninsula Malaysia). We describe the external morphology and colour pattern of the species, which correspond well to the original description, itself based only on two preserved specimens. We performed an in-depth molecular characterisation of the species, including its complete mitochondrial genome, the 18S sequence and elongation 1-alpha (EF1-α) sequence. In addition, EF1-α sequences were also retrieved for 5 additional geoplanid species. No tRNA-Thr could be detected in the mitogenome of B. admarginatum, a lack already reported in several species of geoplanids, but we found a 13 bp sequence that contains the anticodon loop and seems to be conserved among geoplanids and might thus possibly represent a non-canonical undetected tRNA. We discuss the difficulties encountered in trying to reconstruct the cluster of nuclear ribosomal genes, a problem already mentioned for other Triclads. Three phylogenies, based respectively on all mitochondrial proteins, 18S, and EF1-α, were computed; the position of B. admarginatum within the Bipaliinae was confirmed in each tree, as sister-group to various bipaliine species according to the sequences available for each tree. In the mitochondrial proteins tree, which had high support, B. admarginatum was sister to Bipalium kewense and Diversibipalium multilineatum.

 

References

  1. Almeida, A.L., Francoy, T.M., Álvarez-Presas, M. & Carbayo, F. (2021) Convergent evolution: A new subfamily for bipaliin-like Chilean land planarians (platyhelminthes). Zoologica Scripta, 50, 500–508. https://doi.org/10.1111/zsc.12479
  2. Álvarez-Presas, M. & Riutort, M. (2014) Planarian (Platyhelminthes, Tricladida) diversity and molecular markers: a new view of an old group. Diversity, 6, 323–338. https://doi.org/10.3390/d6020323
  3. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S. & Prjibelski, A.D. (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455–477. https://doi.org/10.1089/cmb.2012.0021
  4. Bernt, M., Donath, A., Jühling, F., Externbrink, F., Florentz, C., Fritzsch, G., Pütz, J., Middendorf, M. & Stadler, P.F. (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69, 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
  5. Boratyn, G.M., Schäffer, A.A., Agarwala, R., Altschul, S.F., Lipman, D.J. & Madden, T.L. (2012) Domain enhanced lookup time accelerated BLAST. Biology Direct, 7, 1–14. https://doi.org/10.1186/1745-6150-7-12
  6. Breugelmans, K., Quintana Cardona, J., Artois, T., Jordaens, K. & Backeljau, T. (2012) First report of the exotic blue land planarian, Caenoplana coerulea (Platyhelminthes, Geoplanidae), on Menorca (Balearic Islands, Spain). Zookeys, 199, 91–105. https://doi.org/10.3897/zookeys.199.3215
  7. Capella-Gutiérrez, S., Silla-Martínez, J.M. & Gabaldón, T. (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics, 25, 1972–1973. https://doi.org/10.1093/bioinformatics/btp348
  8. Carbayo, F., Alvarez-Presas, M., Jones, H.D. & Riutort, M. (2016) The true identity of Obama (Platyhelminthes: Geoplanidae) flatworm spreading across Europe. Zoological Journal of the Linnean Society, 177, 5–28. https://doi.org/10.1111/zoj.12358
  9. Carbayo, F., Álvarez-Presas, M., Olivares, C.T., Marques, F.P., Froehlich, E.M. & Riutort, M. (2013) Molecular phylogeny of Geoplaninae (Platyhelminthes) challenges current classification: proposal of taxonomic actions. Zoologica Scripta, 42, 508–528. https://doi.org/10.1111/zsc.12019
  10. Carranza, S., Baguña, J. & Riutort, M. (1999) Origin and evolution of paralogous rRNA gene clusters within the flatworm family Dugesiidae (Platyhelminthes, Tricladida). Journal of Molecular Evolution, 49, 250–259. https://doi.org/10.1007/pl00006547
  11. Carranza, S., Giribet, G., Ribera, C., Baguña, J. & Riutort, M. (1996) Evidence that two types of 18S rDNA coexist in the genome of Dugesia (Schmidtea) mediterranea (Platyhelminthes, Turbellaria, Tricladida). Molecular Biology and Evolution, 13, 824–832. https://doi.org/10.1093/oxfordjournals.molbev.a025643
  12. Crooks, G.E., Hon, G., Chandonia, J.-M. & Brenner, S.E. (2004) WebLogo: a sequence logo generator. Genome research, 14, 1188–1190. https://doi.org/10.1101/gr.849004
  13. Darriba, D., Posada, D., Kozlov, A. M., Stamatakis, A., Morel, B. & Flouri, T. (2019) ModelTest-NG: A new and scalable tool for the selection of DNA and protein evolutionary models. Molecular Biology and Evolution, 37, 291–294. https://doi.org/10.1093/molbev/msz189
  14. De Beauchamp, P. (1933) Planaires terrestres du Raffles Museum. Bulletin of the Raffles Museum, 8, 109–120, pl.
  15. Fourcade, Y., Winsor, L. & Justine, J.-L. (2022) Hammerhead worms everywhere? Modelling the invasion of bipaliin flatworms in a changing climate. Diversity and Distributions, 28, 844–858. https://doi.org/10.1111/ddi.13489
  16. Gastineau, R. & Justine, J.-L. (2020) Complete mitogenome of the invasive land flatworm Parakontikia ventrolineata, the second Geoplanidae (Platyhelminthes) to display an unusually long cox2 gene. Mitochondrial DNA, Part B, 5, 2115–2116. https://doi.org/10.1080/23802359.2020.1765709
  17. Gastineau, R., Justine, J.-L., Lemieux, C., Turmel, M. & Witkowski, A. (2019) Complete mitogenome of the giant invasive hammerhead flatworm Bipalium kewense. Mitochondrial DNA Part B, 4, 1343–1344. https://doi.org/10.1080/23802359.2019.1596768
  18. Gastineau, R., Lemieux, C., Turmel, M. & Justine, J.-L. (2020) Complete mitogenome of the invasive land flatworm Platydemus manokwari. Mitochondrial DNA, Part B, 5, 1689–1690. https://doi.org/10.1080/23802359.2020.1748532
  19. Gastineau, R., Winsor, L. & Justine, J.-L. (2022) The complete mitogenome of the potentially invasive flatworm Australopacifica atrata (Platyhelminthes, Geoplanidae) displays unusual features common to other Rhynchodeminae. Zookeys, 1110, 121–133. https://doi.org/10.3897/zookeys.1110.83228
  20. Glez-Peña, D., Gómez-Blanco, D., Reboiro-Jato, M., Fdez-Riverola, F. & Posada, D. (2010) ALTER: program-oriented conversion of DNA and protein alignments. Nucleic Acids Research, 38, W14–W18. https://doi.org/10.1093/nar/gkq321
  21. Jühling, F., Pütz, J., Florentz, C. & Stadler, P.F. (2012) Armless mitochondrial tRNAs in Enoplea (Nematoda). RNA Biology, 9, 1161–1166. https://doi.org/10.4161/rna.21630
  22. Jühling, T., Duchardt-Ferner, E., Bonin, S., Wöhnert, J., Pütz, J., Florentz, C., Betat, H., Sauter, C. & Mörl, M. (2018) Small but large enough: structural properties of armless mitochondrial tRNAs from the nematode Romanomermis culicivorax. Nucleic Acids Research, 46, 9170–9180. https://doi.org/10.1093/nar/gky593
  23. Justine, J.-L., Gastineau, R., Gros, P., Ruzzier, E., Charles, L. & Winsor, L. (2022a) Hammerhead flatworms (Platyhelminthes, Geoplanidae, Bipaliinae): mitochondrial genomes and description of two new species from France, Italy, and Mayotte. PeerJ, 10, e12725 https://doi.org/10.7717/peerj.12725
  24. Justine, J.-L., Gey, D., Thévenot, J., Gastineau, R. & Jones, H.D. (2020a) The land flatworm Amaga expatria (Geoplanidae) in Guadeloupe and Martinique: new reports and molecular characterization including complete mitogenome. PeerJ, 8, e10098. https://doi.org/10.7717/peerj.10098
  25. Justine, J.-L., Gey, D., Vasseur, J., Thévenot, J., Coulis, M. & Winsor, L. (2021) Presence of the invasive land flatworm Platydemus manokwari (Platyhelminthes, Geoplanidae) in Guadeloupe, Martinique and Saint Martin (French West Indies). Zootaxa, 4951 (2), 381–390. https://doi.org/10.11646/zootaxa.4951.2.11
  26. Justine, J.-L., Winsor, L., Gey, D., Gros, P. & Thévenot, J. (2018) Giant worms chez moi! Hammerhead flatworms (Platyhelminthes, Geoplanidae, Bipalium spp., Diversibipalium spp.) in metropolitan France and overseas French territories. PeerJ, 6, e4672. http://doi.org/10.7717/peerj.4672
  27. Justine, J.-L., Marie, A. D., Gastineau, R., Fourcade, Y. & Winsor, L. (2022b) The invasive land flatworm Obama nungara in La Réunion, a French island in the Indian Ocean, the first report of the species for Africa. Zootaxa, 5154 (4), 469–476. https://doi.org/10.11646/zootaxa.5154.4.4
  28. Justine, J.-L., Winsor, L., Barrière, P., Fanai, C., Gey, D., Han, A.W.K., La Quay-Velázquez, G., Lee, B.P.Y.H., Lefevre, J.M., Meyer, J.Y., Philippart, D., Robinson, D.G., Thévenot, J. & Tsatsia, F. (2015) The invasive land planarian Platydemus manokwari (Platyhelminthes, Geoplanidae): records from six new localities, including the first in the USA. PeerJ, 3, e1037. https://doi.org/10.7717/peerj.1037
  29. Justine, J.-L., Winsor, L., Gey, D., Gros, P. & Thévenot, J. (2020b) Obama chez moi! The invasion of metropolitan France by the land planarian Obama nungara (Platyhelminthes, Geoplanidae). PeerJ, 8, e8385. https://doi.org/10.7717/peerj.8385
  30. Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. https://doi.org/10.1093/molbev/mst010
  31. Kawahara, A.Y., Martinez, J.I., Plotkin, D., Markee, A., Butterwort, V., Couch, C.D. & Toussaint, E.F.A. (2023) Mezcal worm in a bottle: DNA evidence suggests a single moth species. PeerJ, 11, e14948. https://doi.org/10.7717/peerj.14948
  32. Kawakatsu, M., Makino, N. & Shirasawa, Y. (1982) Bipalium nobile sp. nov. (Turbellaria, Tricladida, Terricola), a new land planarian from Tokyo. Annotationes Zoologicae Japonense, 55, 236–262.
  33. Krahn, N., Fischer, J.T. & Söll, D. (2020) Naturally occurring tRNAs with non-canonical structures. Frontiers in Microbiology, 11, 596914. https://doi.org/10.3389/fmicb.2020.596914
  34. Laslett, D. & Canbäck, B. (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics, 24, 172–175. https://doi.org/10.1093/bioinformatics/btm573
  35. Lohse, M., Drechsel, O., Kahlau, S. & Bock, R. (2013) OrganellarGenomeDRAW—a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Research, 41, W575–W581. https://doi.org/10.1093/nar/gkt289
  36. Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A. & Lanfear, R. (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Molecular Biology and Evolution, 37, 1530–1534. https://doi.org/10.1093/molbev/msaa015
  37. Müller, J. (1902) Ein Beitrag zur Kenntnis der Bipaliiden. Zeitschrift für wissenschaftliche Zoologie, 73, 75–114.
  38. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A. & Huelsenbeck, J.P. (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. https://doi.org/10.1093/sysbio/sys029
  39. Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M. & Söding, J. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Molecular systems biology, 7, 539. https://doi.org/10.1038/msb.2011.75
  40. Sluys, R. (2016) Invasion of the Flatworms. American Scientist, 104, 288–295. https://doi.org/10.15112016.122.288
  41. Smith, S.A. & Dunn, C.W. (2008) Phyutility: a phyloinformatics tool for trees, alignments and molecular data. Bioinformatics, 24, 715–716. https://doi.org/10.1093/bioinformatics/btm619
  42. Solà, E., Álvarez-Presas, M., Frías-López, C., Littlewood, D.T.J., Rozas, J. & Riutort, M. (2015) Evolutionary analysis of mitogenomes from parasitic and free-living flatworms. PLoS ONE, 10, e0120081. https://doi.org/10.1371/journal.pone.0120081
  43. Wende, S., Platzer, E.G., Jühling, F., Pütz, J., Florentz, C., Stadler, P.F. & Mörl, M. (2014) Biological evidence for the world's smallest tRNAs. Biochimie, 100, 151–158. https://doi.org/10.1016/j.biochi.2013.07.034
  44. Winsor, L. (1983) A revision of the Cosmopolitan land planarian Bipalium kewense Moseley, 1878 (Turbellaria: Tricladida: Terricola). Zoological Journal of the Linnean Society, 79, 61–100. https://doi.org/10.1111/j.1096-3642.1983.tb01161.x

How to Cite

Soo, O.Y.M., Gastineau, R., Verdon, G., Winsor, L. & Justine, J.-L. (2023) Rediscovery of Bipalium admarginatum de Beauchamp, 1933 (Platyhelminthes, Tricladida, Geoplanidae) in Malaysia, with molecular characterisation including the mitogenome. Zootaxa, 5277 (3), 585–599. https://doi.org/10.11646/zootaxa.5277.3.11