How to get into bones: Proton pump and carbonic anhydrase in Osedax boneworms

Tohoku Journal of Experimental Medicine

Volumn 230, Issue 1, 2013, Pages

  Tresguerres, Martin ^a   Katz, Sigrid ^a   Rouse, Greg W ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Acid secretion; Osteoclast; Siboglinidae; Whale fall

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE; HYDROGEN; PROTON PUMP; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ACID SECRETION; AEROBIC METABOLISM; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BONE REMODELING; CATALYSIS; CONTROLLED STUDY; CONVERGENT EVOLUTION; CYTOPLASM VESICLE; ENZYME ACTIVITY; EPITHELIUM CELL; FEMALE; NONHUMAN; OSEDAX; OSTEOCLAST; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIBOGLINIDAE; STRUCTURE ANALYSIS; ANATOMY AND HISTOLOGY; ANIMAL; BONE; CYTOPLASM; METABOLISM; PHYSIOLOGY; POLYCHAETA; SYMBIOSIS; WHALE;

ADSORPTION; BONE; CONVERGENT EVOLUTION; CYTOPLASMIC INCOMPATIBILITY; ENZYME ACTIVITY; HETEROTROPHY; MEMBRANE; METABOLISM; POLYCHAETE; PUMP; SEAFLOOR; SECRETION; SYMBIONT; WHALE;

BACTERIA (MICROORGANISMS); CETACEA; MAMMALIA; OSEDAX; SIBOGLINIDAE; VERTEBRATA;

ANIMALS; BONE AND BONES; CARBONIC ANHYDRASES; CYTOPLASM; EPITHELIAL CELLS; FEMALE; POLYCHAETA; SYMBIOSIS; VACUOLAR PROTON-TRANSLOCATING ATPASES; WHALES;

EID: 84878341876     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1098/rspb.2013.0625     Document Type: Article

References (60)

1. Rouse GW, Goffredi SK, Vrijenhoek RC. 2004 Osedax: bone-eating marine worms with dwarf males. Science 305, 668-671. (doi:10.1126/science. 1098650)
2. Jones WJ, Johnson SB, Rouse GW, Vrijenhoek RC. 2008 Marine worms (genus Osedax) colonize cow bones. Proc. R. Soc. B 275, 387-391. (doi:10.1098/ rspb.2007.1437)
3. Rouse GW, Goffredi SK, Johnson SB, Vrijenhoek RC. 2011 Not whale-fall specialists, Osedax worms also consume fishbones. Biol. Lett. 7, 736-739. (doi:10. 1098/rsbl.2011.0202)
4. Goffredi SK, Orphan VJ, Rouse GW, Jahnke L, Embaye T, Turk K, Lee R, Vrijenhoek RC. 2005 Evolutionary innovation: a bone-eating marine symbiosis. Environ. Microbiol. 7, 1369-1378. (doi:10.1111/j.1462-2920.2005.00824.x)
5. 2+ sensing by the osteoclast. Cell Calcium 14, 271-277. (doi:10.1016/0143-4160(93)90048-B)
6. Worsaae K, Rouse GW. 2010 The simplicity of males: progenetic dwarf males of four species of Osedax (Annelida) investigated by multi-stainings and CLSM analysis. J. Morphol. 271, 127-142. (doi:10.1002/jmor.10786)
7. Zaidi M et al. 1993 Role of the endothelial cell in osteoclast control: new perspectives. Bone 14, 97-102. (doi:10.1016/8756-3282(93)90234-2)
8. Pomponi SA. 1979 Ultrastructure of cells associated with excavation of calcium carbonate substrates by boring sponges. J. Mar. Biol. Assoc. UK 59, 777-784. (doi:10.1017/S0025315400045756)
9. Pomponi SA. 1980 Cytological mechanisms of calcium carbonate excavation by sponges. Int. Rev. Cytol. 65, 301-319. (doi:10.1016/S0074- 7696(08)61963-4)
10. Clelland E, Saleuddin A. 2000 Vacuolar-type ATPase in the accessory boring organ of Nucella lamellosa (Gmelin) (Mollusca: Gastropoda): role in shell penetration. Biol. Bull. 198, 272-283. (doi:10. 2307/1542530)
11. Webb RS, Saleuddin ASM. 1977 Role of enzymes in the mechanism of shell penetration by the muricid gastropod, Thais lapillus (L.). Can. J. Zool. 55, 1846-1857. (doi:10.1139/z77-238)
12. Chughtai I, Kinght-Jones EW. 1988 Burrowing into limestone by sabellid polychaetes. Zool. Scripta 17, 231-238. (doi:10.1111/j.1463-6409.1988.tb00098.x)
13. Hutchings PA. 2008 Role of polychaetes in bioerosion of coral substrates. In Current developments in bioerosion (eds M Wisshak, L Tapanila), pp. 249-264. Berlin, Germany: Springer.
14. Katz S, Klepal W, Bright M. 2010 The skin of Osedax (Siboglinidae, Annelida): an ultrastructural investigation of its epidermis. J. Morphol. 271, 1272-1280. (doi:10.1002/jmor.10873)
15. Katz S, Klepal W, Bright M. 2011 The Osedax trophosome: organization and ultrastructure. Biol. Bull. 220, 128-139.
16. Higgs ND, Glover AG, Dahlgren TG, Little CTS. 2011 Bone-boring worms: characterizing the morphology, rate, and method of bioerosion by Osedax mucofloris (Annelida, Siboglinidae). Biol. Bull. 221, 307-316.
17. Goffredi SK, Johnson S, Vrijenhoek RC. 2007 Genetic diversity and potential function of microbial symbionts associated with newly discovered species of Osedax polychaete worms. Appl. Environ. Microbiol. 73, 2314-2323. (doi:10.1128/AEM. 01986-06)
18. Zaidi M et al. 1993 Osteoclast function and its control. Exp. Physiol. 78, 721-739.
19. Blair H, Teitelbaum S, Ghiselli R, Gluck S. 1989 Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 245, 855-857. (doi:10.1126/ science.2528207)
20. + ATPase: molecular structure and function, physiological roles and regulation. J. Exp. Biol. 209, 577-589. (doi:10.1242/jeb.02014)
21. Brown D, Breton S. 1996 Mitochondria-rich, proton-secreting epithelial cells. J. Exp. Biol. 199, 2345-2358.
22. Castagna M, Shayakul C, Trotti D, Sacchi VF, Harvey WR, Hediger MA. 1997 Molecular characteristics of mammalian and insect amino acid transporters: implications for amino acid homeostasis. J. Exp. Biol. 200, 269-286.
23. 2+ redistribution, and divalent cation modulation. J. Cell Physiol. 155, 120- 129. (doi:10.1002/jcp. 1041550116)
24. Vrijenhoek RC, Johnson SB, Rouse GW. 2009 A remarkable diversity of bone-eating worms (Osedax; Siboglinidae; Annelida). BMC Evol. Biol. 7, 74. (doi:10.1186/1741-7007-7-74)
25. Moonga BS, Pazianas M, Alam AS, Shankar VS, Huang CL, Zaidi M. 1993 Stimulation of a Gs-like G protein in the osteoclast inhibits bone resorption but enhances tartrate-resistant acid phosphatase secretion. Biochem. Biophys. Res. Commun. 190, 496- 501. (doi:10.1006/bbrc. 1993.1075)
26. Tresguerres M, Parks SK, Salazar E, Levin LR, Goss GG, Buck J. 2010 Bicarbonate-sensing soluble adenylyl cyclase is an essential sensor for acid/base homeostasis. Proc. Natl Acad. Sci. USA 107, 442-447. (doi:10.1073/pnas.0911790107)
27. Pietrement C, Sun-Wada GH, Da Silva N, McKee M, Marshansky V, Brown D, Futai M, Breton S. 2006 Distinct expression patterns of different subunit Isoforms of the V-ATPase in the rat epididymis. Biol. Reprod. 74, 185-194. (doi:10.1095/Biolreprod. 105.043752)
28. Paunescu TG, Jones AC, Tyszkowski R, Brown D. 2008 V-ATPase expression in the mouse olfactory epithelium. Am. J. Physiol. Cell Physiol. 295, C923-C930. (doi:10.1152/Ajpcell.00237.2008)
29. Perry S, Braun M, Genz J, Vulesevic B, Taylor J, Grosell M, Gilmour K. 2010 Acid-base regulation in the plainfin midshipman (Porichthys notatus): an aglomerular marine teleost. J. Comp. Physiol. B 180, 1213-1225. (doi:10.1007/s00360-010-0492-8)
30. Rouse G, Wilson N, Goffredi S, Johnson S, Smart T, Widmer C, Young C, Vrijenhoek R. 2009 Spawning and development in Osedax boneworms (Siboglinidae, Annelida). Mar. Biol. 156, 395-405. (doi:10.1007/s00227-008-1091-z)
31. +-ATPase and NHE2 immunoreactivity in the gill epithelium of the Pacific hagfish (Epatretus stoutii). Comp. Biochem. Physiol. A 145, 312-321. (doi:10.1016/j.cbpa.2006. 06.045)
32. +-ATPase. Comp. Biochem. Physiol. A 148, 133- 141. (doi:10.1016/j.cbpa.2007.03.032)
33. +-ATPase and NHE2 in response to acid and base infusions in the Pacific spiny dogfish (Squalus acanthias). J. Exp. Biol. 208, 345 -354. (doi:10. 1242/jeb.01382)
34. +-ATPase to the basolateral membrane in the Pacific spiny dogfish (Squalus acanthias): a role in base secretion. J. Exp. Biol. 209, 599-609. (doi:10. 1242/jeb.02059)
35. +-ATPase translocation during blood alkalosis in dogfish gills: interaction with carbonic anhydrase and involvement in the postfeeding alkaline tide. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292, R2012-R2019. (doi:10.1152/ajpregu.00814.2006)
36. Tresguerres M, Katoh F, Orr E, Parks SK, Goss GG. 2006 Chloride uptake and base secretion in freshwater fish: a transepithelial ion-transport metabolon? Physiol. Biochem. Zool. 79, 981-996. (doi:10.1086/507658)
37. +-ATPase and band 3 anion exchanger in rabbit collecting duct intercalated cells. Am. J. Physiol. Renal Physiol. 260, F506-F517.
38. Brown D, Sabolic I, Gluck S. 1992 Polarized targeting of V-atpase in kidney epithelial-cells. J. Exp. Biol. 172, 231-243.
39. Huusgaard RS, Vismann B, Kuhl M, Macnaugton M, Colmander V, Rouse GW, Glover AG, Dahlgren T, Worsaae K. 2012 The potent respiratory system of Osedax mucofloris (Siboglinidae, Annelida): a prerequisite for the origin of bone-eating Osedax? PLoS ONE 7, e35975. (doi:10.1371/journal.pone. 0035975)
40. Bright M, Lallier FH. 2010 The biology of vestimentiferan tubeworms. In Oceanography and marine biology: an annual review (eds RN Gibson, RJA Atkinson, JDM Gordon), pp. 213-266. London, UK: Taylor & Francis.
41. Goffredi SK, Childress JJ, Desaulniers NT, Lee RW, Lallier FH, Hammond D. 1997 Inorganic carbon acquisition by the hydrothermal vent tubeworm Riftia pachyptila depends upon high external PCO2 and upon proton elimination by the worm. J. Exp. Biol. 200, 883-896.
42. Goffredi SK, Childress JJ. 2001 Activity and inhibitor sensitivity of ATPases in the hydrothermal vent tubeworm Riftia pachyptila: a comparative approach. Mar. Biol. 138, 259-265. (doi:10.1007/ s002270000462)
43. + elimination in the hydrothermal vent tube-worm Riftia pachyptila. Cahiers de Biologie Marine 39, 297-300.
44. 2 shift. Physiol. Biochem. Zool. 72, 296-306. (doi:10. 1086/316664)
45. Goffredi SK, Girguis PR, Childress JJ, Desaulniers NT. 1999 Physiological functioning of carbonic anhydrase in the hydrothermal vent tubeworm Riftia pachyptila. Biol. Bull. 196, 257-264. (doi:10. 2307/1542950)
46. Arp AJ, Childress JJ, Fisher CR. 1985 Blood gas transport in Riftia pachyptila. Bull. Biol. Soc. Wash. 6, 289-300.
47. Freytag JK, Girguis PR, Bergquist DC, Andras JP, Childress JJ, Fisher CR. 2001 A paradox resolved: sulfide acquisition by roots of seep tubeworms sustains net chemoautotrophy. Proc. Natl Acad. Sci. USA 98, 13 408 - 13 413. (doi:10.1073/pnas. 231589498)
48. Julian D, Gaill F, Wood E, Arp AJ, Fisher CR. 1999 Roots as a site of hydrogen sulfide uptake in the hydrocarbon seep vestimentiferan Lamellibrachia sp. J. Exp. Biol. 202, 2245-2257.
49. Dando PR, Southward AJ, Southward EC, Lamont P, Harvey R. 2008 Interactions between sediment chemistry and frenulate pogonophores (Annelida) in the north-east Atlantic. Deep Sea Res. I Oceanogr. Res. Pap. 55, 966-996. (doi:10.1016/j.dsr.2008. 04.002)
50. +ATPase. J. Cell Biol. 105, 1637-1648. (doi:10. 1083/jcb.105.4.1637)
51. Cordes EE, Arthur MA, Shea K, Arvidson RS, Fisher CR. 2005 Modeling the mutualistic interactions between tubeworms and microbial consortia. PLoS Biol. 3, e77. (doi:10.1371/journal.pbio.0030077)
52. Dattagupta S, Arthur MA, Fisher CR. 2008 Modification of sediment geochemistry by the hydrocarbon seep tubeworm Lamellibrachia luymesi: a combined empirical and modeling approach. Geochim. Cosmochim. Acta 72, 2298-2315. (doi:10. 1016/j.gca.2008.02.016)
53. Dattagupta S, Miles LL, Barnabei MS, Fisher CR. 2006 The hydrocarbon seep tubeworm Lamellibrachia luymesi primarily eliminates sulfate and hydrogen ions across its roots to conserve energy and ensure sulfide supply. J. Exp. Biol. 209, 3795-3805. (doi:10.1242/jeb.02413)
54. Manahan DT, Wright SH, Stephens GC, Rice MA. 1982 Transport of dissolved amino acids by the mussel, Mytilus edulis: demonstration of net uptake from natural seawater. Science 215, 1253-1255. (doi:10.1126/science.215.4537.1253)
55. Stephens GC. 1963 Uptake of organic material by aquatic invertebrates. II. Accumulation of amino acids by the bamboo worm, Clymenella Torquata. Comp. Biochem. Physiol. 10, 191 - 202. (doi:10. 1016/0010-406X(63)90033-1)
56. Fontaine AR, Chia FS. 1968 Echinoderms: an autoradiographic study of assimilation of dissolved organic molecules. Science 161, 1153-1155. (doi:10.1126/science.161.3846.1153)
57. Gomme J. 1982 Epidermal nutrient absorption in marine invertebrates: a comparative analysis. Am. Zool. 22, 691-708. (doi:10.1093/ icb/22.3.691)
58. Glover CN, Bucking C, Wood CM. 2011 Adaptations to in situ feeding: novel nutrient acquisition pathways in an ancient vertebrate. Proc. R. Soc. B 278, 3096-3101. (doi:10.1098/Rspb.2010.2784)
59. Nesbitt SA, Horton MA. 1997 Trafficking of matrix collagens through bone-resorbing osteoclasts. Science 276, 266-269. (doi:10.1126/science.276. 5310.266)
60. Fujikura K, Fujiwara Y, Kawato M. 2006 A new species of Osedax (annelida: siboglinidae) associated with whale carcasses off Kyushu, Japan. Zool. Sci. 23, 733-740. (doi:10.2108/zsj.23.733)