Table of Contents
International Journal of Evolutionary Biology
Volume 2015, Article ID 538918, 11 pages
http://dx.doi.org/10.1155/2015/538918
Research Article

The Evolutionary History of Daphniid α-Carbonic Anhydrase within Animalia

1Program in Ecology & Evolutionary Biology, Department of Biology, University of Oklahoma, 730 Van Vleet Oval, Norman, OK 73019, USA
2University of Oklahoma Biological Station, 15389 Station Road, Kingston, OK 73439, USA
3Murray State College, One Murray Campus, Tishomingo, OK 73460, USA

Received 5 October 2014; Revised 12 March 2015; Accepted 14 March 2015

Academic Editor: Hirohisa Kishino

Copyright © 2015 Billy W. Culver and Philip K. Morton. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. D. Tortell, “Evolutionary and ecological perspectives on carbon acquisition in phytoplankton,” Limnology and Oceanography, vol. 45, no. 3, pp. 744–750, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. N. G. Hairston Jr., C. L. Holtmeier, W. Lampert et al., “Natural selection for grazer resistance to toxic cyanobacteria: evolution of phenotypic plasticity?” Evolution, vol. 55, no. 11, pp. 2203–2214, 2001. View at Publisher · View at Google Scholar · View at Scopus
  3. P. D. Jeyasingh, A. Ragavendran, S. Paland, J. A. Lopez, R. W. Sterner, and J. K. Colbourne, “How do consumers deal with stoichiometric constraints? Lessons from functional genomics using Daphnia pulex,” Molecular Ecology, vol. 20, no. 11, pp. 2341–2352, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Urabe, J. Togari, and J. J. Elser, “Stoichiometric impacts of increased carbon dioxide on a planktonic herbivore,” Global Change Biology, vol. 9, no. 6, pp. 818–825, 2003. View at Publisher · View at Google Scholar · View at Scopus
  5. H. G. Pollard, J. K. Colbourne, and W. Keller, “Reconstruction of centuries-old Daphnia communities in a lake recovering from acidification and metal contamination,” Ambio, vol. 32, no. 3, pp. 214–218, 2003. View at Google Scholar · View at Scopus
  6. C. M. G. Martins, D. V. Almeida, L. F. F. Marins, and A. Bianchini, “mRNA expression and activity of ion-transporting proteins in gills of the blue crab Callinectes sapidus: effects of waterborne copper,” Environmental Toxicology and Chemistry, vol. 30, no. 1, pp. 206–211, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. W. J. O'Brien and F. deNoyelles Jr., “Photosynthetically elevated pH as a factor in zooplankton mortality in nutrient enriched ponds,” Ecology, vol. 53, no. 4, pp. 605–614, 1972. View at Publisher · View at Google Scholar
  8. K. E. Havens, “Acidification effects on the plankton size spectrum: an in situ mesocosm experiment,” Journal of Plankton Research, vol. 14, no. 12, pp. 1687–1696, 1992. View at Publisher · View at Google Scholar · View at Scopus
  9. A. M. Derry and S. E. Arnott, “Adaptive reversals in acid tolerance in copepods from lakes recovering from historical stress,” Ecological Applications, vol. 17, no. 4, pp. 1116–1126, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Erlandsson, N. Cory, J. Fölster et al., “Increasing dissolved organic carbon redefines the extent of surface water acidification and helps resolve a classic controversy,” BioScience, vol. 61, no. 8, pp. 614–618, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Moya, L. Huisman, E. E. Ball et al., “Whole transcriptome analysis of the coral acropora millepora reveals complex responses to CO2-driven acidification during the initiation of calcification,” Molecular Ecology, vol. 21, no. 10, pp. 2440–2454, 2012. View at Publisher · View at Google Scholar · View at Scopus
  12. R. G. Eppinger, P. H. Briggs, C. Dusel-Bacon et al., “Environmental geochemistry at Red Mountain, an unmined volcanogenic massive sulphide deposit in the Bonnifield district, Alaska Range, east-central Alaska,” Geochemistry: Exploration, Environment, Analysis, vol. 7, no. 3, pp. 207–223, 2007. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Satake, A. Oyagi, and Y. Iwao, “Natural acidification of lakes and rivers in Japan: the ecosystem of Lake Usoriko (pH 3.4-3.8),” Water, Air, and Soil Pollution, vol. 85, no. 2, pp. 511–516, 1995. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Ezoe, C. H. Lin, M. Noto, Y. Watanabe, and K. Yoshimura, “Evolution of water chemistry in natural acidic environments in Yangmingshan, Taiwan,” Journal of Environmental Monitoring, vol. 4, no. 4, pp. 533–540, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. T. Georgalis, S. F. Perry, and K. M. Gilmour, “The role of branchial carbonic anhydrase in acid-base regulation in rainbow trout (Oncorhynchus mykiss),” Journal of Experimental Biology, vol. 209, no. 3, pp. 518–530, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. T.-Y. Lin, B.-K. Liao, J.-L. Horng, J.-J. Yan, C.-D. Hsiao, and P.-P. Hwang, “Carbonic anhydrase 2-like a and 15a are involved in acid-base regulation and Na+ uptake in zebrafish H+-ATPase-rich cells,” The American Journal of Physiology—Cell Physiology, vol. 294, no. 5, pp. C1250–C1260, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. K. M. Gilmour and S. F. Perry, “Carbonic anhydrase and acid-base regulation in fish,” The Journal of Experimental Biology, vol. 212, no. 11, pp. 1647–1661, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. R. P. Henry and J. N. Cameron, “The role of Carbonic Anhydrase in respiration, ion regulation and acid-base balance in the aquatic crab Callinectes sapidus and the terrestrial crab Gecarnicus lateralis,” The Journal of Experimental Biology, vol. 103, pp. 205–223, 1983. View at Google Scholar
  19. R. P. Henry, “The role of carbonic anhydrase in blood ion and acid-base regulation,” American Zoologist, vol. 24, no. 1, pp. 241–251, 1984. View at Publisher · View at Google Scholar · View at Scopus
  20. P. D. Cooper, “Mechanisms of hemolymph acid-base regulation in aquatic insects,” Physiological Zoology, vol. 67, no. 1, pp. 29–53, 1994. View at Google Scholar
  21. M. R. Badger and G. D. Price, “The role of carbonic anhydrase in photosynthesis,” Annual Review of Plant Physiology and Plant Molecular Biology, vol. 45, pp. 369–392, 1994. View at Publisher · View at Google Scholar · View at Scopus
  22. A. K. Weber and R. Pirow, “Physiological responses of Daphnia pulex to acid stress,” BMC Physiology, vol. 9, no. 1, article 9, 25 pages, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. S. L. Teitelbaum, “Bone resorption by osteoclasts,” Science, vol. 289, no. 5484, pp. 1504–1508, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. N. Le Roy, D. J. Jackson, B. Marie, P. Ramos-Silva, and F. Marin, “The evolution of metazoan α-carbonic anhydrases and their roles in calcium carbonate biomineralization,” Frontiers in Zoology, vol. 11, article 75, pp. 1–16, 2014. View at Publisher · View at Google Scholar
  25. D. Hewett-Emmett and R. E. Tashian, “Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families,” Molecular Phylogenetics and Evolution, vol. 5, no. 1, pp. 50–77, 1996. View at Publisher · View at Google Scholar · View at Scopus
  26. A. K.-C. So and G. S. Espie, “Cyanobacterial carbonic anhydrases,” Canadian Journal of Botany, vol. 83, no. 7, pp. 721–734, 2005. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Aspatwar, M. E. E. Tolvanen, and S. Parkkila, “Phylogeny and expression of carbonic anhydrase-related proteins,” BMC Molecular Biology, vol. 11, article 25, 19 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. K. Fasseas, D. Tsikou, E. Flemetakis, and P. Katinakis, “Molecular and biochemical analysis of the β class carbonic anhydrases in Caenorhabditis elegans,” Molecular Biology Reports, vol. 37, no. 6, pp. 2941–2950, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. P. J. Linser, K. E. Smith, T. J. Seron, and M. N. Oviedo, “Carbonic anhydrases and anion transport in mosquito midgut pH regulation,” Journal of Experimental Biology, vol. 212, no. 11, pp. 1662–1671, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. Y. Xu, L. Feng, P. D. Jeffrey, Y. Shi, and F. M. M. Morel, “Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms,” Nature, vol. 452, no. 6, pp. 56–62, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. J. K. Colbourne, M. E. Pfrender, D. Gilbert et al., “The ecoresponsive genome of Daphnia pulex,” Science, vol. 331, no. 6017, pp. 555–561, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Lynch and J. S. Conery, “The evolutionary fate and consequences of duplicate genes,” Science, vol. 290, no. 5494, pp. 1151–1155, 2000. View at Publisher · View at Google Scholar · View at Scopus
  33. J. Näsvall, L. Sun, J. R. Roth, and D. I. Andersson, “Real-time evolution of new genes by innovation, amplification, and divergence,” Science, vol. 338, no. 6105, pp. 384–387, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. K. Tamura, D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar, “MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods,” Molecular Biology and Evolution, vol. 28, no. 10, pp. 2731–2739, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. E. M. Gerts, Y.-K. Yu, R. Agarwala, A. A. Schäffer, and S. F. Altschul, “Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST,” BMC Biology, vol. 4, article 41, 2006. View at Publisher · View at Google Scholar · View at Scopus
  36. M. A. Larkin, G. Blackshields, N. P. Brown et al., “Clustal W and Clustal X version 2.0,” Bioinformatics, vol. 23, no. 21, pp. 2947–2948, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Whelan and N. Goldman, “A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach,” Molecular Biology and Evolution, vol. 18, no. 5, pp. 691–699, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. M. A. Miller, W. Pfeiffer, and T. Schwartz, “Creating the CIPRES Science Gateway for inference of large phylogenetic trees,” in Proceedings of the Gateway Computing Environments Workshop (GCE '10), pp. 1–8, New Orleans, La, USA, November 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Ronquist and J. P. Huelsenbeck, “MrBayes 3: Bayesian phylogenetic inference under mixed models,” Bioinformatics, vol. 19, no. 12, pp. 1572–1574, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Stamatakis, “RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies,” Bioinformatics, vol. 30, no. 9, pp. 1312–1313, 2014. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Rambaut, FigTree v1.3.1: Tree Figure Drawing Site, FigTree Website, 2009.
  42. A. Krogh, B. Larsson, G. von Heijne, and E. L. L. Sonnhammer, “Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes,” Journal of Molecular Biology, vol. 305, no. 3, pp. 567–580, 2001. View at Publisher · View at Google Scholar · View at Scopus
  43. O. Emanuelsson, S. Brunak, G. von Heijne, and H. Nielsen, “Locating proteins in the cell using TargetP, SignalP and related tools,” Nature Protocols, vol. 2, no. 4, pp. 953–971, 2007. View at Publisher · View at Google Scholar · View at Scopus
  44. N. Fankhauser and P. Mäser, “Identification of GPI anchor attachment signals by a Kohonen self-organizing map,” Bioinformatics, vol. 21, no. 9, pp. 1846–1852, 2005. View at Publisher · View at Google Scholar · View at Scopus
  45. A. J. Esbaugh and B. L. Tufts, “The structure and function of carbonic anhydrase isozymes in the respiratory system of vertebrates,” Respiratory Physiology & Neurobiology, vol. 154, no. 1-2, pp. 185–198, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Hilvo, M. Tolvanen, A. Clark et al., “Characterization of CA XV, a new GPI-anchored form of carbonic anhydrase,” Biochemical Journal, vol. 392, no. 1, pp. 83–92, 2005. View at Publisher · View at Google Scholar · View at Scopus
  47. K. S. Smith and J. G. Ferry, “Prokaryotic carbonic anhydrases,” FEMS Microbiology Reviews, vol. 24, no. 4, pp. 335–366, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Hoegg, H. Brinkmann, J. S. Taylor, and A. Meyer, “Phylogenetic timing of the fish-specific genome duplication correlates with the diversification of teleost fish,” Journal of Molecular Evolution, vol. 59, no. 2, pp. 190–203, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. A. Meyer and Y. van de Peer, “From 2R to 3R: evidence for a fish-specific genome duplication (FSGD),” BioEssays, vol. 27, no. 9, pp. 937–945, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. K. F. Rewitz and L. I. Gilbert, “Daphnia Halloween genes that encode cytochrome P450s mediating the synthesis of the arthropod molting hormone: evolutionary implications,” BMC Evolutionary Biology, vol. 8, no. 1, article 60, 8 pages, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. F. A. Kondrashov, “Gene duplication as a mechanism of genomic adaptation to a changing environment,” Proceedings of the Royal Society B: Biological Sciences, vol. 279, no. 1749, pp. 5048–5057, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. International Aphid Genomics Consortium, “Genome sequence of the pea aphid Acyrthosiphon pisum,” PLoS Biology, vol. 8, no. 2, Article ID e1000313, 24 pages, 2010. View at Publisher · View at Google Scholar
  53. J.-C. Simon, M. E. Pfrender, R. Tollrian, D. Tagu, and J. K. Colbourne, “Genomics of environmentally induced phenotypes in 2 extremely plastic arthropods,” Journal of Heredity, vol. 102, no. 5, pp. 512–525, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. T. G. Evans, F. Chan, B. A. Menge, and G. E. Hofmann, “Transcriptomic responses to ocean acidification in larval sea urchins from a naturally variable pH environment,” Molecular Ecology, vol. 22, no. 6, pp. 1609–1625, 2013. View at Publisher · View at Google Scholar · View at Scopus