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Evolution of gene order in mtDNA of Baikal endemic amphipods and its possible mechanisms

https://doi.org/10.18699/vjgb-26-15

Abstract

Significant gene order diversity of mitochondrial (mt) genomes of invertebrates is peculiar to subphylum Crustacea, and to order Amphipoda in particular. Amphipods from Lake Baikal are also known as a group with unique gene orders in their mt genomes. To estimate the diversity of protein-coding gene orders (GOs) in amphipods, a comparative analysis of gene rearrangements in the mt genomes of Baikal and non-Baikal species was performed. In some cases, gene rearrangement data and the history of gene relocation in different taxonomic groups can also supplement the results of phylogenetic inferences. Among the thirteen mt genomes of Baikal species sequenced in previous studies, four gene order patterns were identified, and fourteen gene order patterns for 114 mt genomes of non-Baikal species were observed. The type and number of rearrangement steps (from 1 to 3) required to transition from one order to another and the number of mt genes rearranged in each GO (from 1 to 5) were also defined. Baikalian amphipods belong to two lineages (I and II) according to molecular data which reveal their origin from two independent introductions of ancestral species into the lake. All cases of mt gene order rearrangements have been detected in species from the first lineage, whereas the mt gene order in the second lineage is conserved in all species studied and corresponds to the Pancrustacean pattern (PanGO). PanGO has been determined as the ancestral gene order for both Baikalian amphipod lineages. The possible mechanisms of mt gene order rearrangements such as a complete or partial duplication of mt genome and subsequent random deletions are discussed in our study. It is supposed that increased mutation rate, weakening of stabilizing selection and other specific factors may influence the probability of emergence and fixation of different GOs in mt genomes of Baikalian amphipods. 

About the Authors

E. A. Sirotinina
Limnological Institute of the Siberian Branch of the Russian Academy of Sciences
Russian Federation

Irkutsk



D. Yu. Sherbakov
Limnological Institute of the Siberian Branch of the Russian Academy of Sciences
Russian Federation

Irkutsk



E. V. Romanova
Limnological Institute of the Siberian Branch of the Russian Academy of Sciences
Russian Federation

Irkutsk



References

1. Abascal F., Zardoya R., Telford M.J. TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res. 2010;38(Suppl. 2):W7-W13. doi 10.1093/nar/gkq291

2. Basso A., Babbucci M., Pauletto M., Riginella E., Patarnello T., Negrisolo E. The highly rearranged mitochondrial genomes of the crabs Maja crispata and Maja squinado (Majidae) and gene order evolution in Brachyura. Sci Rep. 2017;7(1):4096. doi 10.1038/s41598-017-04168-9

3. Benito J.B., Porter M.L., Niemiller M.L. Comparative mitogenomic analysis of subterranean and surface amphipods (Crustacea, Amphipoda) with special reference to the family Crangonyctidae. BMC Genomics. 2024;25(1):298. doi 10.1186/s12864-024-10111-w

4. Bernt M., Merkle D., Ramsch K., Fritzsch G., Perseke M., Bernhard D., Schlegel M., Stadler P.F., Middendorf M. CREx: inferring genomic rearrangements based on common intervals. Bioinformatics. 2007; 23(21):2957-2958. doi 10.1093/bioinformatics/btm468

5. Boore J.L. Animal mitochondrial genomes. Nucleic Acids Res. 1999; 27(8):1767-1780. doi 10.1093/nar/27.8.1767

6. Bukin Yu.S., Petunina J.V., Sherbakov D.Yu. The mechanisms for genetic diversity of Baikal endemic amphipod Gmelinoides fasciatus: relationships between the population processes and paleoclimatic history of the lake. Russ J Genet. 2018;54(9):1059-1068. doi 10.1134/S1022795418090053

7. Castellucci F., Luchetti A., Mantovani B. Exploring mitogenome evolution in Branchiopoda (Crustacea) lineages reveals gene order rearrangements in Cladocera. Sci Rep. 2022;12(1):4931. doi 10.1038/s41598-022-08873-y

8. Charlesworth B. Fundamental concepts in genetics: effective population size and patterns of molecular evolution and variation. Nat Rev Genet. 2009;10(3):195-205.

9. Drozdova P.B., Madyarova E.V., Gurkov A.N., Saranchina A.E., Romanova E.V., Petunina J.V., Peretolchina T.E., Sherbakov D.Y., Timofeyev M.A. Lake Baikal amphipods and their genomes, great and small. Vavilov J Genet Breed. 2024;28(3):317-325. doi 10.18699/vjgb-24-36

10. Fourdrilis S., de Frias Martins A.M., Backeljau T. Relation between mitochondrial DNA hyperdiversity, mutation rate and mitochondrial genome evolution in Melarhaphe neritoides (Gastropoda: Littorinidae) and other Caenogastropoda. Sci Rep. 2018;8(1):17964. doi 10.1038/s41598-018-36428-7

11. Fučíková K., Lewis P.O., González-Halphen D., Lewis L.A. Gene arrangement convergence, diverse intron content, and genetic code modifications in mitochondrial genomes of Sphaeropleales (Chlorophyta). Genome Biol Evol. 2016;6(8):2170-2180. doi 10.1093/gbe/evu172

12. Goldberg E.L., Chebykin E.P., Zhuchenko N.A., Vorobyeva S.S., Stepanova O.G., Khlystov O.M., Ivanov E.V., Weinberg E., Gvozdkov A.N. Uranium isotopes as proxies of the environmental history of the Lake Baikal watershed (East Siberia) during the past 150ka. Palaeogeogr Palaeoclimatol Palaeoecol. 2010;294(1-2):16-29. doi 10.1016/j.palaeo.2009.08.030

13. Gouy M., Guindon S., Gascuel O. SeaView Version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol. 2010;27(2):221-224. doi 10.1093/molbev/msp259

14. Hartmann T., Bernt M., Middendorf M. An exact algorithm for sorting by weighted preserving genome rearrangements. IEEE/ACM Trans Comput Biol Bioinform. 2019;16(1):52-62. doi 10.1109/TCBB.2018. 2831661

15. Hou Z., Sket B., Li S. Phylogenetic analyses of Gammaridae crustacean reveal different diversification patterns among sister lineages in the Tethyan region. Cladistics. 2014;30(4):352-365. doi 10.1111/cla.12055

16. Jühling F., Pütz J., Bernt M., Donath A., Middendorf M., Florentz C., Stadler P.F. Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Res. 2012;40(7):2833-2845. doi 10.1093/nar/gkr1131

17. Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., Von Haeseler A., Jermiin L.S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14(6):587-589. doi 10.1038/nmeth.4285

18. Kamaltynov R.M. On the higher classification of Lake Baikal amphipods. Crustaceana. 1999;72(8):933-944. doi 10.1163/1568540 99503834

19. Kamaltynov R.M. Amphipods (Amphipoda: Gammaridea). In: Index of Animal Species Inhabiting Lake Baikal and its Catchment Area. Novosibirsk: Nauka Publ., 2001;572-831 (in Russian)

20. Kilpert F., Podsiadlowski L. The complete mitochondrial genome of the common sea slater, Ligia oceanica (Crustacea, Isopoda) bears a novel gene order and unusual control region features. BMC Genomics. 2006;7:241. doi 10.1186/1471-2164-7-241

21. Kilpert F., Held C., Podsiadlowski L. Multiple rearrangements in mitochondrial genomes of Isopoda and phylogenetic implications. Mol Phylogenet Evol. 2012;64(1):106-117. doi 10.1016/j.ympev.2012.03.013

22. Lavrov D.V., Lang B.F. Poriferan mtDNA and animal phylogeny based on mitochondrial gene arrangements. Syst Biol. 2005;54(4):651-659. doi 10.1080/10635150500221044

23. Lavrov D.V., Pett W. Animal mitochondrial DNA as we do not know it: mt-genome organization and evolution in nonbilaterian lineages. Genome Biol Evol. 2016;8(9):2896-2913. doi 10.1093/gbe/evw195

24. Lavrov D.V., Boore J.L., Brown W.M. Complete mtDNA sequences of two millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Mol Biol Evol. 2002; 19(2):163-169. doi 10.1093/oxfordjournals.molbev.a004068

25. Li J.Y., Zeng C., Yan G.Y., He L.S. Characterization of the mitochondrial genome of an ancient amphipod Halice sp. MT-2017 (Pardaliscidae) from 10,908 m in the Mariana Trench. Sci Rep. 2019;9(1): 2610. doi 10.1038/s41598-019-38735-z

26. Mamos T., Grabowski M., Rewicz T., Bojko J., Strapagiel D., Burzyński A. Mitochondrial genomes, phylogenetic associations, and SNP recovery for the key invasive Ponto-Caspian amphipods in Europe. Int J Mol Sci. 2021;22(19):10300. doi 10.3390/ijms221910300

27. Mats V.D., Shcherbakov D.Y., Efimova I.M. Late Cretaceous-Cenozoic history of the Lake Baikal depression and formation of its unique biodiversity. Stratigr Geol Correl. 2011;19(4):404-423. doi 10.1134/S0869593811040058

28. Minh B.Q., Schmidt H.A., Chernomor O., Schrempf D., Woodhams M.D., Von Haeseler A., Lanfear R., Teeling E. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37(5):1530-1534. doi 10.1093/molbev/msaa015

29. Moreno-Carmona M., Cameron S.L., Prada Quiroga C.F. How are the mitochondrial genomes reorganized in Hexapoda? Differential evolution and the first report of convergences within Hexapoda. Gene. 2021;791:145719. doi 10.1016/j.gene.2021.145719

30. Mueller R.L., Boore J.L. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Mol Biol Evol. 2005;22(10):2104-2112. doi 10.1093/molbev/msi204

31. Nissanka N., Minczuk M., Moraes C.T. Mechanisms of mitochondrial DNA deletion formation. Trends Genet. 2019;35(3):235-244. doi 10.1016/j.tig.2019.01.001

32. Oliveira M.T., Pontes C.B., Ciesielski G.L. Roles of the mitochondrial replisome in mitochondrial DNA deletion formation. Genet Mol Biol. 2020;43(Suppl. 1):e20190069. doi 10.1590/1678-4685-GMB2019-0069

33. Pääbo S., Thomas W.K., Whitfield K.M., Kumazawa Y., Wilson A.C. Rearrangements of mitochondrial transfer RNA genes in marsupials. J Mol Evol. 1991;33(5):426-430. doi 10.1007/BF02103134

34. Petunina J.V., Vavrischuk N.V., Bukin Yu.S., Romanova E.V. Variability of morphological and genetic characteristics of Macrohectopus branickii (Dyb., 1874) (Amphipoda, Macrohectopidae). Izvestiya Irkutskogo Gosudarstvennogo Universiteta. Seriya: Biologiya. Ecologiya = The Bulletin of Irkutsk State University. Series: Biology. Ecology. 2023;46:18-28. doi 10.26516/2073-3372.2023.46.18 (in Russian)

35. Rambaut A. FigTree. Latest Version – v1.4.4. 2018. Available at: http://tree.bio.ed.ac.uk/software/figtree/

36. Rivarola-Duarte L., Otto C., Jühling F., Schreiber S., Bedulina D., Jakob L., Gurkov A., … Sartoris F., Pörtner H.O., Timofeyev M., Luckenbach T., Stadler P.F. A first Glimpse at the genome of the Baikalian amphipod Eulimnogammarus verrucosus. J Exp Zool B Mol Dev Evol. 2014;322(3):177-189. doi 10.1002/jez.b.22560

37. Romanova E.V., Sherbakov D.Y. Different rates of molecular evolution of mitochondrial genes in Baikalian and non-Baikalian amphipods. Limnol Freshwater Biol. 2019;(6):339-344. doi 10.31951/2658-3518-2019-A-6-339

38. Romanova E.V., Aleoshin V.V., Kamaltynov R.M., Mikhailov K.V., Logacheva M.D., Sirotinina E.A., Gornov A.Y., Anikin A.S., Sherbakov D.Y. Evolution of mitochondrial genomes in Baikalian amphipods. BMC Genomics. 2016;17(Suppl. 14):1016. doi 10.1186/s12864-016-3357-z

39. Romanova E.V., Bukin Y.S., Mikhailov K.V., Logacheva M.D., Aleoshin V.V., Sherbakov D.Y. Hidden cases of tRNA gene duplication and remolding in mitochondrial genomes of amphipods. Mol Phylogenet Evol. 2020;144:106710. doi 10.1016/j.ympev.2019.106710

40. Romanova E.V., Bukin Y.S., Mikhailov K.V., Logacheva M.D., Aleoshin V.V., Sherbakov D.Y. The mitochondrial genome of a freshwater pelagic amphipod Macrohectopus branickii is among the longest in Metazoa. Genes (Basel). 2021;12(12):2030. doi 10.3390/genes12122030

41. Shao R., Dowton M., Murrell A., Barker S.C. Rates of gene rearrangement and nucleotide substitution are correlated in the mitochondrial genomes of insects. Mol Biol Evol. 2003;20(10):1612-1619. doi 10.1093/molbev/msg176

42. Sherbakov D.Y. Molecular phylogenetic studies on the origin of biodiversity in Lake Baikal. Trends Ecol Evol. 1999;14(3):92-95. doi 10.1016/s0169-5347(98)01543-2

43. Sterling-Montealegre R.A., Prada C.F. Variability and evolution of gene order rearrangement in mitochondrial genomes of arthropods (except Hexapoda). Gene. 2024;892:147906. doi 10.1016/j.gene.2023.147906

44. Tan M.H., Gan H.M., Lee Y.P., Poore G.C.B., Austin C.M. Digging deeper: new gene order rearrangements and distinct patterns of codons usage in mitochondrial genomes among shrimps from the Axiidea, Gebiidea and Caridea (Crustacea: Decapoda). PeerJ. 2017;5: e2982. doi 10.7717/peerj.2982

45. Tan M.H., Gan H.M., Lee Y.P., Bracken-Grissom H., Chan T.Y., Miller A.D., Austin C.M. Comparative mitogenomics of the Decapoda reveals evolutionary heterogeneity in architecture and composition. Sci Rep. 2019;9(1):10756. doi 10.1038/s41598-019-47145-0

46. The Galaxy Community. The Galaxy platform for accessible, reproducible, and collaborative data analyses: 2024 update. Nucleic Acids Res. 2024;52(W1):83-94. https://doi.org/10.1093/nar/gkae410

47. Wang R., Li X., Qi J. The complete paternally inherited mitochondrial genomes of three clam species in genus Macridiscus (Bivalvia: Veneridae): a TDRL model of dimer-mitogenome rearrangement of doubly uniparental inheritance. Front Mar Sci. 2022;9:1016779. doi 10.3389/fmars.2022.1016779

48. Xia Y., Zheng Y., Murphy R.W., Zeng X. Intraspecific rearrangement of mitochondrial genome suggests the prevalence of the tandem duplication-random loss (TDLR) mechanism in Quasipaa boulengeri. BMC Genomics. 2016;17(1):965. doi 10.1186/s12864-016-3309-7

49. Xu W., Jameson D., Tang B., Higgs P.G. The relationship between the rate of molecular evolution and the rate of genome rearrangement in animal mitochondrial genomes. J Mol Evol. 2006;63(3):375-392. doi 10.1007/s00239-005-0246-5

50. Zapelloni F., Jurado-Rivera J.A., Jaume D., Juan C., Pons J. Comparative mitogenomics in Hyalella (Amphipoda: Crustacea). Genes (Basel). 2021;12(2):292. doi 10.3390/genes12020292

51. Zardoya R. Recent advances in understanding mitochondrial genome diversity. F1000Res. 2020;9:270. doi 10.12688/f1000research.21490.1


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