Biodiversity Science ›› 2014, Vol. 22 ›› Issue (1): 80-87.doi: 10.3724/SP.J.1003.2014.13237

Special Issue: From Genome to Diversity

• Orginal Article • Previous Article     Next Article

Biodiversity and adaptive evolution of Antarctic notothenioid fishes

Qianghua Xu1, 3, 4, Zhichao Wu1, 2, Liangbiao Chen1, 2, *()   

  1. 1. College of Marine Sciences, College of Fisheries and Life Sciences, Shanghai Ocean University, Shanghai 201306
    2. Key Laboratory of Aquaculture Resources and Utilization, Ministry of Education, Shanghai 201306
    3. Key Laboratory of Sustainable Exploitation of Oceanic Fisheries Resources, Ministry of Education, Shanghai 201306
    4. National Distant-water Fisheries Engineering Research Center, Shanghai 201306
  • Received:2013-11-07 Accepted:2014-01-17 Online:2014-02-10
  • Chen Liangbiao E-mail:lbchen@shou.edu.cn

The sea surrounding the Antarctic continent is one of the coldest regions in the world. It provides an environmentally unique and isolated “hotbed” for evolution to take place. In the past 30 million years, species of Perciform suborder Notothenioidei evolved and diversified from a benthic and temperate-water ancestor, and now dominate the fish fauna of the coldest ocean. Because of their distribution across temperature zones both inside and outside the Antarctic Polar Front, notothenioid fishes are regarded as excellent model organisms for exploring mechanisms of adaptive evolution, particularly cold adaptation. We first summarize research progress on the biodiversity of Antarctic fish and then review current findings on the peculiar biological characteristics of Antarctic notothenioids that evolved in response to a freezing environment. Research has revealed that extensive gene duplication and transcriptomic changes occurred during the adaptive radiation of notothenioid fish. Examples of highly duplicated genes in the Antarctic lineages include genes encoding hepcidin, and zona pellucida proteins, in addition to various retrotransposable elements. A few genes from Antarctic notothenioid fishes have been used as transgenes and demonstrated to be effective in making transgenic plants cold-hardy. In the coming years, the genomes of some Antarctic notothenioid species will be fully sequenced and the adaptive functions of duplicated genes will be further elucidated. Such studies will deepen our understanding of how genomes evolve in freezing environments, and provide an improved knowledge of molecular mechanisms of cold adaptation.

Key words: the Southern Ocean, Antarctic notothenioid fishes, diversity, adaptive evolution

[1] Acierno R, MacDonald JA, Agnisola C, Tota B (1995) Blood volume in the hemoglobinless Antarctic teleost Chionodraco hamatus (Lönnberg).Journal of Experimental Zoology, 272, 407-409.
[2] Anderson ME (1994) Systematics and osteology of the Zoarcidae (Teleostei: Perciformes), pp. 1-60. Smith Institute of Ichthyology, Grahamstown JLB.
[3] Andriashev AP (1965) A general review of the Antarctic fish fauna.Monograph Biology, 15, 491-550.
[4] Andriashev AP (1991) Possible pathways of Paraliparis (Pisces: Liparididae) and some other North Pacific secondarily deep-sea fishes into North Atlantic and Arctic depths.Polar Biology, 11, 213-218.
[5] Bagis H, Akkoç T, Tasş A, Aktoprakligil D (2008) Cryogenic effect of antifreeze protein on transgenic mouse ovaries and the production of live offspring by orthotopic transplantation of cryopreserved mouse ovaries.Molecular Reproduction and Development, 75, 608-613.
[6] Boron I, Russo R, Boechi L, Cheng CHC, di Prisco G, Estrin DA, Verde C, Nadra AD (2011) Structure and dynamics of Antarctic fish neuroglobin assessed by computer simulations.IUBMB Life, 63, 206-213.
[7] Buckley BA, Place SP, Hofmann GE (2004) Regulation of heat shock genes in isolated hepatocytes from an Antarctic fish, Trematomus bernacchii.Journal of Experimental Biology, 207, 3649-3656.
[8] Cao LX (曹立雪) (2009) Adapative Evolution of the Zona Pellucida Gene Family in Antarctic Notothenioids Fishes (南极Notothenioids鱼类Zona pellucida基因家族的适应性进化). PhD dissertation, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing. (in Chinese with English abstract)
[9] Cheng CHC, Chen LB, Near TJ, Jin Y (2003) Functional antifreeze glycoprotein genes in temperate-water New Zealand nototheniid fish infer an Antarctic evolutionary origin.Molecular Biology and Evolution, 20, 1897-1908.
[10] Cheng CHC, Detrich HW (2007) Molecular ecophysiology of Antarctic notothenioid fishes.Philosophical Transactions of the Royal Society B: Biological Sciences, 362, 2215-2232.
[11] Cheng CHC, di Prisco G, Verde C (2009) Cold-adapted Antarctic fish: the discovery of neuroglobin in the dominant suborder Notothenioidei.Gene, 433, 100-101.
[12] Chen LB, DeVries AL, Cheng CHC (1997) Evolution of antifreeze glycoprotein gene from a trypsinogen gene in Antarctic notothenioid fish. Proceedings of the National Academy of Sciences,USA, 94, 3811-3816.
[13] Chen ZZ, Cheng CHC, Zhang JF, Cao LX, Chen L, Zhou LH, Jin YD, Ye H, Deng C, Dai ZH, Xu QH, Hu P, Sun SH, Shen Y, Chen LB (2008) Transcriptomic and genomic evolution under constant cold in Antarctic notothenioid fish. Proceedings of the National Academy of Sciences,USA, 105, 12944-12949.
[14] Clarke A, Crame JA (1989) The origin of the Southern Ocean marine fauna.Geological Society, London, Special Publications, 47, 253-268.
[15] Cocca E, Ratnayake-Lecamwasam M, Parker SK, Camardella L, Ciaramella M, di Prisco G, Detrich HW (1995) Genomic remnants of alpha-globin genes in the hemoglobinless antarctic icefishes . Proceedings of the National Academy of Sciences,USA, 92, 1817-1821.
[16] Coppe A, Agostini C, Marino IAM, Zane L, Bargellioni L, Bortoluzzi S, Patamello T (2013) Genome evolution in the cold: Antarctic icefish muscle transcriptome reveals selective duplications increasing mitochondrial function.Genome Biology and Evolution, 5, 45-60.
[17] Coppes PZL, Somero GN (2007) Biochemical adaptations of notothenioid fishes: comparisons between cold temperate South American and New Zealand species and Antarctic species.Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 147, 799-807.
[18] De Broyer C, Clarke A, Koubbi P, Pakhomov E, Scott F, VandenBerghe E, Danis B (2013) Register of Antarctic Marine Species. (2013.08.15).
[19] Deng C, Cheng CHC, Ye H, He XM, Chen LB (2010) Evolution of an antifreeze protein by neofunctionalization under escape from adaptive conflict. Proceedings of the National Academy of Sciences,USA, 107, 21593-21598.
[20] Deng G, Andrews DW, Laursen RA (1997) Amino acid sequence of a new type of antifreeze protein, from the longhorn sculpin Myoxocephalus octodecimspinosis.FEBS Letters, 402, 17-20.
[21] Detrich HW, Parker SK, Williams RC, Nogales JE, Downing KH (2000) Cold adaptation of microtubule assembly and dynamics structural interpretation of primary sequence changes present in the α- and β-tubulins of antarctic fishes.Journal of Biological Chemistry, 275, 37038-37047.
[22] di Prisco G, Eastman JT, Giordano D, Parisi E, Verde C (2007) Biogeography and adaptation of notothenioid fish: hemoglobin function and globin gene evolution. Gene, 398, 143-155.
[23] Duman JG, DeVries AL (1976) Isolation, characterization, and physical properties of protein antifreezes from the winter flounder, Pseudopleuronectes americanus.Comparative Biochemistry and Physiology, Part B: Comparative Bioche- mistry, 54, 375-380.
[24] Eastman JT (1993) Antarctic Fish Biology: Evolution in a Unique Environment. Academic Press, San Diego.
[25] Eastman JT (2005) The nature of the diversity of Antarctic fish.Polar Biology, 28, 93-107.
[26] Ewart KV, Fletcher GL (1993) Herring antifreeze protein: primary structure and evidence for a C-type lectin evolutionary origin.Molecular Marine Biology and Biotechnology, 2, 20-27.
[27] Fields PA, Somero GN (1998) Hot spots in cold adaptation: localized increases in conformational flexibility in lactate dehydrogenase A4 orthologs of Antarctic notothenioid fishes. Proceedings of the National Academy of Sciences,USA, 95, 11476-11481.
[28] Francis JE, Poole I (2002) Cretaceous and early Tertiary climates of Antarctica: evidence from fossil wood.Palaeo-geography, Palaeoclimatology, Palaeoecology, 182, 47-64.
[29] Giordano D, Russo R, di Prisco G, Verde C (2012) Molecular adaptations in Antarctic fish and marine microorganisms. Marine Genomics, 6, 1-6.
[30] Gon O, Heemstra PC (1990) Fishes of the Southern Ocean. Smith Institute of Ichthyology, Grahamstown JLB.
[31] Grove TJ, Hendrickson JW, Sidell BD (2004) Two species of Antarctic icefishes (genus Champsocephalus) share a common genetic lesion leading to the loss of myoglobin expression.Polar Biology, 27, 579-585.
[32] Hofmann GE, Buckley BA, Airaksinen S, Keen JE, Somero GN (2000) Heat-shock protein expression is absent in the Antarctic fish Trematomus bernacchii (family Nototh- eniidae).Journal of Experimental Biology, 203, 2331-2339.
[33] Iwami T, Kock KH (1990) Channichthyidae. In: Fishes of the Southern Ocean (eds Gon O, Hemstra PC), pp. 381-399. Smith Institute of Ichthyology, Grahamstown JLB.
[34] Jin Y, DeVries AL (2006) Antifreeze glycoprotein levels in Antarctic notothenioid fishes inhabiting different thermal environments and the effect of warm acclimation.Com-parative Biochemistry and Physiology, Part B, Biochemistry and Molecular Biology, 144, 290-300.
[35] Johnston IA (2003) Muscle metabolism and growth in Antarctic fishes (suborder Notothenioidei): evolution in a cold environment.Comparative Biochemistry and Physiology, Part B: Biochemistry and Molecular Biology, 136, 701-713.
[36] Khanna HK, Daggard GE (2006) Targeted expression of redesigned and codon optimised synthetic gene leads to recrystallisation inhibition and reduced electrolyte leakage in spring wheat at sub-zero temperatures.Plant Cell Report, 25, 1336-1346.
[37] Kimura H, Weisz A, Kurashima Y, Hashimoto K, Ogura T, D’Acquisto F, Addeo R, Makuuchi M, Esumi H (2000) Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide.Blood, 95, 189-197.
[38] Lucassen M, Schmidt A, Eckerle LG, Pörtner HO (2003) Mitochondrial proliferation in the permanent vs. temporary cold: enzyme activities and mRNA levels in Antarctic and temperate zoarcid fish.American Journal of Physiology: Regulatory, Integrative and Comparative Physiology, 285, 1410-1420.
[39] Minning DM, Gow AJ, Bonaventura J, Braun R, Dewhirst M, Goldberg DE, Stamler JS (1999) Ascaris haemoglobin is a nitric oxide-activated ‘deoxygenase’. Nature, 401, 497-502.
[40] Montgomery J, Clements K (2000) Disaptation and recovery in the evolution of Antarctic fishes.Trends in Ecology & Evolution, 15, 267-271.
[41] Near TJ, Parker SK, Detrich HW (2006) A genomic fossil reveals key steps in hemoglobin loss by the antarctic icefishes.Molecular Biology and Evolution, 23, 2008-2016.
[42] Near TJ, Pesavento JJ, Cheng CHC (2004) Phylogenetic investigations of Antarctic notothenioid fishes (Perciformes: Notothenioidei) using complete gene sequences of the mitochondrial encoded 16S rRNA.Molecular Phylogenetics and Evolution, 32, 881-891.
[43] Nisoli E, Falcone S, Tonello C, Cozzi V, Palomba L, Fiorani M, Pisconti A, Brunelli S, Cardile A, Francolini M, Cantoni O, Carruba MO, Moncada S, Clementi E (2004) Mitochondrial biogenesis by NO yields functionally active mitochondria in mammals. Proceedings of the National Academy of Sciences,USA, 101, 16507-16512.
[44] Place SP, Hofmann GE (2001) Temperature interactions of the molecular chaperone Hsc70 from the eurythermal marine gobyGillichthys mirabilis. Journal of Experimental Biology, 204, 2675-2682.
[45] Raymond JA, DeVries AL (1977) Adsorption inhibition as a mechanism of freezing resistance in polar fishes. Proceedings of the National Academy of Sciences,USA, 74, 2589-2593.
[46] Rizzello A, Romano A, Kottra G, Acierno R, Storelli C, Verri T, Daniel H, Maffia M (2013) Protein cold adaptation strategy via a unique seven-amino acid domain in the icefish (Chionodraco hamatus) PEPT1 transporter. Proceedings of the National Academy of Sciences,USA, 110, 7068-7073.
[47] Scher HD, Martin EE (2006) Timing and climatic consequ- ences of the opening of the Drake Passage.Science, 312, 428-430.
[48] Shevenell AE, Kennett JP, Lea DW (2004) Middle Miocene southern ocean cooling and Antarctic cryosphere expansion. Science, 305, 1766-1770.
[49] Sidell BD, O’Brien KM (2006) When bad things happen to good fish: the loss of hemoglobin and myoglobin expression in Antarctic icefishes.Journal of Experimental Biology, 209, 1791-1802.
[50] Skora KE, Neyelov AV (1992) Fish of Admiralty Bay (King George Island, South Shetland Islands, Antarctica).Polar Biology, 12, 469-476.
[51] Somero GN, DeVries AL (1967) Temperature tolerance of some Antarctic fishes.Science, 156, 257-258.
[52] Suri C, McClain J, Thurston G, McDonald DM, Zhou H, Oldmixon EH, Sato TN, Yancopoulos GD (1998) Increased vascularization in mice overexpressing angiopoietin-1.Science, 282, 468-471.
[53] Van de Putte AP, Van Houdt JKJ, Maes GE, Hellemans B, Collins MA, Volckaert FAM (2012) High genetic diversity and connectivity in a common mesopelagic fish of the Southern Ocean: the myctophid Electrona antarctica. Deep Sea Research, Part II, Topical Studies in Oceanography, 59, 199-207.
[54] Verde C, Parisi E, di Prisco G (2006) The evolution of thermal adaptation in polar fish.Gene, 385, 137-145.
[55] Voronina EP, Neelov AV (2001) Structural traits of alimentary tract of fishes of the family Channichthyidae (Nototh- enioidei).Journal of Ichthyology c/c of Voprosy Ikhtiologii, 41, 778-788.
[56] Wallis JG, Wang H, Guerra DJ (1997) Expression of a synthetic antifreeze protein in potato reduces electrolyte release at freezing temperatures.Plant Molecular Biology, 35, 323-330.
[57] Xu QH, Cheng CHC, Hu P, Ye H, Chen ZZ, Cao LX, Chen L, Shen Y, Chen LB (2008) Adaptive evolution of hepcidin genes in antarctic notothenioid fishes.Molecular Biology and Evolution, 25, 1099-1112.
[58] Yang N, Peng C, Cheng D, Huang Q, Xu G, Gao F, Chen L (2013) The over-expression of calmodulin from Antarctic notothenioid fish increases cold tolerance in tobacco.Gene, 521, 32-37.
[59] Zhao Y, Ratnayake-Lecamwasam M, Parker SK, Cocca E, Camardella L, di Prisco G, Detrich HW (1998) The major adult α-globin gene of Antarctic teleosts and its remnants in the hemoglobinless icefishes calibration of the mutational clock for nuclear genes.Journal of Biological Chemistry, 273, 14745-14752.
[1] Ben-Feng HAN Xin Zhou Xue Zhang. (2020) Verification of virus identity and host association using genomics technologies . Biodiv Sci, 28(5): 0-0.
[2] Lintao Huang Hui Huang Lei Jiang. (2020) A revised taxonomy for Chinese hermatypic corals . Biodiv Sci, 28(4): 515-523.
[3] Dan Liu,Zhongling Guo,Xiaoyang Cui,Chunnan Fan. (2020) Comparison of five associations of Taxus cuspidata and their species diversity . Biodiv Sci, 28(3): 340-349.
[4] Jinyuan Su,Yu Yan,Chong Li,Dan Li,Fang K. Du. (2020) Informing conservation strategies with genetic diversity in Wild Plant with Extremely Small Populations: A review on gymnosperms . Biodiv Sci, 28(3): 376-384.
[5] Kai Wang,Jinlong Ren,Hongman Chen,Zhitong Lyu,Xianguang Guo,Ke Jiang,Jinmin Chen,Jiatang Li,Peng Guo,Yingyong Wang,Jing Che. (2020) The updated checklists of amphibians and reptiles of China . Biodiv Sci, 28(2): 189-218.
[6] Xia Li,Wanze Zhu,Shouqin Sun,Shumiao Shu,Zheliang Sheng,Jun Zhang,Ting Liu,Zhicai Zhang. (2020) Influence of habitat on the distribution pattern and diversity of plant community in dry and warm valleys of the middle reaches of the Dadu River, China . Biodiv Sci, 28(2): 117-127.
[7] Yisheng Ma,Qingqing Ma,Nianjun He,Dapeng Zhu,Kaihui Zhao,Hongcai Liu,Shuai Li,Liang Sun,Liubin Tang. (2020) Camera-trapping survey of mammals and birds in the Foping National Nature Reserve, China . Biodiv Sci, 28(2): 226-230.
[8] Zhenyuan Liu,Xingliang Meng,Zhengfei Li,Junqian Zhang,Jing Xu,Senlu Yin,Zhicai Xie. (2020) Diversity assessment and protection strategies for the mollusk community in the southern Dongting Lake . Biodiv Sci, 28(2): 155-165.
[9] Gongguo Li,Ping Li,Hangying Xu,Haiyan Yu,Jian Yu. (2020) Path analysis of zooplankton diversity and environmental factors in the water sources rivers, Zhejiang Province . Biodiv Sci, 28(2): 166-175.
[10] Minxia Liu,Quandi Li,Xiaoxuan Jiang,Sujuan Xia,Xiaoning Nan,Yaya Zhang,Bowen Li. (2020) Contribution of rare species to species diversity and species abundance distribution pattern in the Gannan subalpine meadow . Biodiv Sci, 28(2): 107-116.
[11] Xiongwei Yang,Ankang Wu,Qixian Zou,Guangrong Li,Mingming Zhang,Canshi Hu,Haijun Su. (2020) Field monitoring of mammals and birds using infrared cameras in Mayanghe National Nature Reserve, Guizhou, China . Biodiv Sci, 28(2): 219-225.
[12] Haiou Liu,Fengchun Zhang,Fuwei Zhao,Leshan Du,Dayuan Xue. (2020) Biodiversity sensitive issues from changes in the strategic objectives of the financial mechanism for the Convention on Biological Diversity . Biodiv Sci, 28(2): 244-252.
[13] Yijia Geng,Yu Tian,Junsheng Li,Jing Xu. (2020) Progress and prospects of the Post-2020 Global Biodiversity Framework . Biodiv Sci, 28(2): 238-243.
[14] Wenying Zhuang,Yi Li,Huandi Zheng,Zhaoqing Zeng,Xincun Wang. (2020) Threat status of non-lichenized macro-ascomycetes in China and its threatening factors . Biodiv Sci, 28(1): 26-40.
[15] DING Wei,WANG Yu-Bing,XIANG Guan-Hai,CHI Yong-Gang,LU Shun-Bao,ZHENG Shu-Xia. (2020) Effects of Caragana microphylla encroachment on community structure and ecosystem function of a typical steppe . Chin J Plant Ecol, 44(1): 33-43.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed