Skip to main content
SpringerLink
Log in

Patterns of organic osmolytes in two marine bivalves, Macoma balthica, and Mytilus spp., along their European distribution

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Patterns of nine intracellular free amino acids (FAA), which are utilized as organic osmolytes for salinity-induced cell volume regulation in marine osmoconformers, were compared in five Macoma balthica populations and seven Mytilus spp. populations along their European distribution. Three types of FAA patterns were classified within both taxa: a northern Baltic type, a southern Baltic type and an Atlantic/Mediterranean type which mainly differ regarding the share of alanine and taurine. Differences are discussed in relation to habitat salinity and population genetics. Along a salinity gradient, the total size of the intracellular FAA pool did not differ between sympatric M. balthica and Mytilus spp., and was significantly correlated with habitat osmolality in a range from 70 to 600 mmol kg−1 H2O (oligohaline to mesohaline) in both bivalves. In M. balthica, this correlation was mainly based on significant correlations of alanine (15–100 mmol kg−1 DW), glycine (30–100 mmol kg−1 DW) and taurine (0–70 mmol kg−1 DW) with habitat osmolality. In Mytilus spp., only glycine (25–100 mmol kg−1 DW) and taurine (4–180 mmol kg−1 DW) were significantly correlated with habitat osmolality. The concentration of alanine was three times lower in Mytilus spp. than in M. balthica and did not correlate with habitat osmolality. Within a habitat osmolality range from 600 to 1,100 mmol kg−1 H2O (mesohaline to marine) the concentration of FAA remained constant in both taxa. It is suggested that under marine conditions additional organic osmolytes must become more important for cell volume regulation in Macoma and Mytilus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Baginski RM, Pierce SK (1977) Time course of intracellular free amino-acid accumulation in tissues of Modiolus demissus during high salinity adaptation. Comp Biochem Phys A 57:407–412

    Article  CAS  Google Scholar 

  • Bishop JS, Burton RS (1993) Amino-acid synthesis during hyperosmotic stress in Penaeus-aztecus postlarvae. Comp Biochem Phys A 106:49–56

    Article  Google Scholar 

  • Bishop SH, Ellis LL, Burcham JM (1983) Amino acid metabolism in molluscs. In: Wilbur KM (ed) The Mollusca. Metabolism biochemistry and molecular biomechanics, vol 1. Academic, New York, pp 243–327

  • Bishop SH, Greenwalt DE, Kapper MA, Paynter KT, Ellis LL (1994) Metabolic regulation of proline, glycine, and alanine accumulation as intracellular osmolytes in ribbed mussel gill tissue. J Exp Zool 268:151–161

    Article  CAS  Google Scholar 

  • Blank M, Bastrop R, Rohner M, Jurss K (2004) Effect of salinity on spatial distribution and cell volume regulation in two sibling species of Marenzelleria (Polychaeta: Spionidae). Mar Ecol Prog Ser 271:193–205

    Article  Google Scholar 

  • De Goeij P, Luttikhuizen P (1998) Deep-burying reduces growth in intertidal bivalves: field and mesocosm experiments with Macoma balthica. J Exp Mar Biol Ecol 228:327–337

    Article  Google Scholar 

  • De Vooys CGN (1991) Anaerobic metabolism in sublittoral living Mytilus galloprovincialis in the Mediterranean—4. Role of amino acids in adaptation to low salinities during anaerobiosis and aerobiosis. Comp Biochem Phys 100A:423–431

    Google Scholar 

  • De Vooys CGN, Holwerda DA (1986) Anaerobic metabolism in sublittoral living Mytilus galloprovincialis an the Mediterranean. III. The effect of anoxia and osmotic stress on some kinetic parameters of adductor muscle pyruvate kinase. Comp Biochem Phys B 85:217–221

    Article  Google Scholar 

  • De Vooys CGN, Geenevasen JAJ (2002) Biosynthesis and role in osmoregulation of glycine-betaine in the Mediterranean mussel Mytilus galloprovincialis LMK. Comp Biochem Phys B 132:409–414

    Google Scholar 

  • De Zwaan A (1991) Molluscs. In: Bryant C (ed) Metazoan life without oxygen. Chapman and Hall, London, pp 186–217

    Google Scholar 

  • Deaton LE (2001) Hyperosmotic volume regulation in the gills of the ribbed mussel, Geukensia demissa: rapid accumulation of betaine and alanine. J Exp Mar Biol Ecol 260:185–197

    Article  PubMed  CAS  Google Scholar 

  • Dupaul WD, Webb KL (1971) Free amino acid accumulation in isolated gill tissue of Mya arenaria. Arch Int Physiol Biochim 79:327–336

    Article  PubMed  CAS  Google Scholar 

  • Gardner JPA (1996) The Mytilus edulis species complex in southwest England: Effects of hybridization and introgression upon interlocus associations and morphometric variation. Mar Biol 125:385–399

    Article  Google Scholar 

  • Gardner JPA, Thompson RJ (2001) The effects of coastal and estuarine conditions on the physiology and survivorship of the mussels Mytilus edulis, M. trossulus and their hybrids. J Exp Mar Biol Ecol 265:119–140

    Article  Google Scholar 

  • Gilles R (1987) Volume regulation in cells of euryhaline invertebrates. Curr Top Membr Transp 30:205–247

    CAS  Google Scholar 

  • Goolish EM, Burton RS (1989) Energetics of osmoregulation in an intertidal copepod—effects of anoxia and lipid reserves on the pattern of free amino-acid accumulation. Func Ecol 3:81–89

    Article  Google Scholar 

  • Gosling E (1992) Genetics. In: Gosling EM (ed) The Mussel Mytilus: ecology, physiology, genetics and culture. Elsevier, Amsterdam, pp 309–382

    Google Scholar 

  • Henry RP, Mangum CP, Webb KL (1980) Salt and water balance in the oligohaline clam Rangia cuneta. II Accumulation of intracellular free amino acids during high salinity adaptation. J Exp Zool 211:11–29

    Article  CAS  Google Scholar 

  • Hülsmann R, Osinsky R, Schiedek D, Schöttler U (1991) The importance of proline metabolism for adaptation to low salinity in Nereis diversicolor (Polychaeta). Verh Deut Zool Gesell 84:411

    Google Scholar 

  • Hummel H, Colucci F, Bogaards RH, Strelkov P (2001) Genetic traits in the bivalve Mytilus from Europe, with an emphasis on Arctic populations. Pol Biol 24:44–52

    Article  Google Scholar 

  • Jagnow B, Gosselck F (1987) Bestimmungsschlüssel für die Gehäuseschnecken und Muscheln der Ostsee. Mitt Zool Mus 63:191–268

    Google Scholar 

  • Koehn RK (1991) The genetics and taxonomy of species in the genus Mytilus. Aquaculture 94:125–145

    Article  Google Scholar 

  • Koenig ML, Powell EN, Kasschau MR (1981) The effects of salinity change on the free amino-acid pools of 2 nereid polychaetes, Neanthes succinea and Leonereis culveri. Comp Biochem Phys A 70:631–637

    Article  Google Scholar 

  • Luttikhuizen PC, Drent J, Baker AJ (2003) Disjunct distribution of highly diverged mitochondrial lineage clade and population subdivision in a marine bivalve with pelagic larval dispersal. Mol Ecol 12:2215–2229

    Article  PubMed  CAS  Google Scholar 

  • Matson SE, Davis JP, Chew KK (2003) Laboratory hybridization of the mussels, Mytilus trossulus and M. galloprovincialis: larval growth, survival and early development. J Shellfish Res 22:423–430

    Google Scholar 

  • Matsushima O, Hayashi YS (1992) Metabolism of d-alanine and l-alanine and regulation of intracellular free amino-acid levels during salinity stress in a brackish-water bivalve Corbicula japonica. Comp Biochem Phys A 102:465–471

    Article  Google Scholar 

  • McDonald JH, Seed R, Koehn RK (1991) Allozymes and morphometric characters of three species of Mytilus in the Northern and Southern Hemispheres. Mar Biol 111:323–333

    Article  Google Scholar 

  • Peng KW, Chew SF, Ip YK (1994) Free amino-acids and cell-volume regulation in the sipunculid Phascolosoma arcuatum. Physiol Zool 67:580–597

    CAS  Google Scholar 

  • Pierce SK, Warren JW (2001) The taurine efflux portal used to regulate cell volume in response to hypoosmotic stress seems to be similar in many cell types: Lessons to be learned from molluscan red blood cells. Am Zool 41:710–720

    Article  CAS  Google Scholar 

  • Pierce SK, Rowland-Faux LM, O'Brian SM (1992) Different salinity tolerance mechanisms in Atlantic and Chesapeake Bay conspecific oysters—glycine betaine and amino-acid pool variations. Mar Biol 113:107–115

    Article  CAS  Google Scholar 

  • Pierce SK, Rowland-Faux LM, Crombie BN (1995) The mechanism of glycine betaine regulation in response to hyperosmotic stress in oyster mitochondria—a comparative-study of Atlantic and Chesapeake Bay oysters. J Exp Zool 271:161–170

    Article  CAS  Google Scholar 

  • Qiu JW, Tremblay R, Bourget E (2002) Ontogenetic changes in hyposaline tolerance in the mussels Mytilus edulis and M. trossulus: implications for distribution. Mar Ecol Prog Ser 228:143–152

    Article  Google Scholar 

  • Riginos C, Cunningham CW (2005) Local adaptation and species segregation in two mussel (Mytilus edulis x Mytilus trossulus) hybrid zones. Mol Ecol 14:381–400

    Article  PubMed  CAS  Google Scholar 

  • Sanjuan A, Zapata C, Alvarez G (1994) Mytilus galloprovincialis and M. edulis on the coasts of the Iberian Peninsula. Mar Ecol Prog Ser 113:131–146

    Article  Google Scholar 

  • Sanjuan A, Zapata C, Alvarez G (1997) Genetic differentiation in Mytilus galloprovincialis Lmk. throughout the world. Ophelia 47:13–31

    Google Scholar 

  • Schiedek D (1997) Marenzelleria viridis (Verrill, 1873) (Polychaeta), a new benthic species within European coastal waters. Some metabolic features. J Exp Mar Biol Ecol 211:85–101

    Article  Google Scholar 

  • Seed R (1992) Systematics evolution and distribution of mussels belonging to the genus Mytilus: an overview. Am Malacol Bull 9:123–137

    Google Scholar 

  • Shumway SE, Gabbott PA, Youngson A (1977) Effect of fluctuating salinity on concentrations of free amino-acids and ninhydrin-positive substances in adductor muscles of 8 species of bivalve mollusks. J Exp Mar Biol Ecol 29:131–150

    Article  CAS  Google Scholar 

  • Smietanka B, Zbawicka M, Wolowicz M, Wenne R (2004) Mitochondrial DNA lineages in the European populations of mussels (Mytilus spp.). Mar Biol 146:79–92

    Article  CAS  Google Scholar 

  • Sokolowski A, Wolowicz M, Hummel H (2003) Free amino acids in the clam Macoma balthica L. (Bivalvia, Mollusca) from brackish waters of the southern Baltic Sea. Comp Biochem Physiol A 134:579–592

    Google Scholar 

  • Somero GN, Yancey PH (1997) Osmolytes and cell volume regulation: physiological and evolutionary principles. In: Danztler W (ed) Handbook of physiology, section 14: cell physiology, vol II. Oxford University Press, New York, pp 1445–1477

  • Theede H (1984) Physiological approaches to environmental problems of the Baltic. Limnologica 15:443–458

    CAS  Google Scholar 

  • Vaeinoelae R (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Mar Biol 143:935–946

    Article  Google Scholar 

  • Vaeinoelae R, Varvio SL (1989) Biosystematics of Macoma balthica in northwestern Europe 23. In: European marine biological symposium, Swansea (UK), 1988

  • Vaeinoelae R, Hvilsom MM (1991) Genetic divergence and a hybrid zone between Baltic and North Sea Mytilus populations (Mytilidae: Mollusca). Biol J Linn Soc 43:127–148

    Article  Google Scholar 

  • Welborn JR, Manahan DT (1995) Taurine metabolism in larvae of marine molluscs (Bivalvia, Gastropoda). J Exp Biol 198:1791–1799

    PubMed  CAS  Google Scholar 

  • Wiedmeyer VT, Porterfield SP, Hendrich SP (1982) Quantification of dns-amino acids from body tissues and fluids using high performance liquid chromatography. J Chromatogr 231:410

    Article  PubMed  Google Scholar 

  • Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830

    Article  PubMed  CAS  Google Scholar 

  • Zurburg W, De Zwaan A (1981) The role of amino-acids in anaerobiosis and osmoregulation in bivalves. J Exp Zool 215:315–325

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge A. Pronker, C. Sola, M. Markiegi, P. Garcia Meunier, V. Bequet Buren, R. Lasota, A. Sokolowski, E. Flach, G. Ejdung, S. Govella and P. Magni for their help during the field sampling campaigns. We wish to thank H. Hummel and R. Bastrop for their invaluable comments to an earlier draft of the manuscript. This study was funded by the European Commission (Research Directorate General, Environment Programme-Marine Ecosystems) in the Community’s Fifth Framework Programme (BIOCOMBE project, contract EVK3-2001-00146).

Author information

Authors and Affiliations

  1. Baltic Sea Research Institute Warnemuende, Seestrasse 15, 18119, Rostock, Germany

    Sandra Kube, Anke Gerber & Doris Schiedek

  2. Netherlands Institute of Ecology, Centre for Estuarine and Marine Ecology, Korringaweg 7, 4401, Yerseke, The Netherlands

    Jeroen M. Jansen

Authors
  1. Sandra Kube
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anke Gerber
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jeroen M. Jansen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Doris Schiedek
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sandra Kube.

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kube, S., Gerber, A., Jansen, J.M. et al. Patterns of organic osmolytes in two marine bivalves, Macoma balthica, and Mytilus spp., along their European distribution. Mar Biol 149, 1387–1396 (2006). https://doi.org/10.1007/s00227-006-0303-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-006-0303-7

Keywords

Search

Navigation