Skip to main content

The Unusual Response of Encysted Embryos of the Animal Extremophile, Artemia franciscana, to Prolonged Anoxia

  • Chapter
  • First Online:
Anoxia

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 21))

Abstract

Encysted embryos (cysts) of the brine shrimp, Artemia franciscana, appear to bring their overall metabolism to a reversible standstill during prolonged anoxia. Mechanisms involved in this unusual response are considered, along with the broader significance of cells that survive in the absence of measurable free energy flow and macromolecular turnover, when fully hydrated and at physiological temperature.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P (eds) (2002) Artemia: basic and applied biology. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Anchordouguy TJ, Hand SC (1994) Acute blockage of the ubiquitin-mediated proteolytic pathway during invertebrate quiescence. Am J Physiol 267:R895–R900

    Google Scholar 

  • Anchordouguy TJ, Hand SC (1995) Reactivation of ubiquination in Artemia franciscana embryos during recovery from anoxia-induced quiescence. J Exp Biol 198:1299–1305

    Google Scholar 

  • Berjak P (2006) Unifying perspectives of some mechanisms basic to desiccation tolerance across life forms. Seed Sci Res 16:1–15

    Article  CAS  Google Scholar 

  • Browne RA, Sorgeloos P, Trotman CNA (eds) (1991) Artemia biology. CRC Press, Boca Raton

    Google Scholar 

  • Busa WB, Crowe JH, Matson GB (1982) Intracellular pH and the metabolic status of dormant and developing Artemia embryos. Arch Biochem Biophys 216:711–718

    Article  PubMed  CAS  Google Scholar 

  • Chen T, Amons R, Clegg JS, Warner AH, MacRae TH (2003) Molecular characterization of artemin and ferritin from Artemia franciscana. Eur J Biochem 270:137–145

    Article  PubMed  CAS  Google Scholar 

  • Chen T, Villeneuve TS, Garant KA, Amons R, MacRae TH (2007) Functional characterization of artemin, a ferritin homolog synthesized in Artemia embryos during encystment and diapause. FEBS J 274:1093–1101

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS (1992) Post-anoxic viability and developmental rate of Artemia franciscana encysted embryos. J Exp Biol 169:255–260

    Google Scholar 

  • Clegg JS (1994) The unusual response of Artemia franciscana embryos to anoxia. J Exp Zool 270:332–334

    Article  Google Scholar 

  • Clegg JS (1997) Embryos of Artemia franciscana survive four years of continuous anoxia: the case for complete metabolic rate depression. J Exp Biol 200:467–475

    PubMed  Google Scholar 

  • Clegg JS (2001) Cryptobiosis–a peculiar state of biological organization. Comp Biochem Physiol B 128:613–624

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS (2007) Protein stability in Artemia embryos during prolonged anoxia. Biol Bull 212:74–81

    Article  PubMed  CAS  Google Scholar 

  • Clegg J, Conte FP (1980) A review of the cellular and developmental biology of Artemia. In: Persoone G, Sorgeloos P, Roels O, Jaspers E (eds) The brine shrimp artemia, vol 2. Universa Press, Wetteren, pp 11–54

    Google Scholar 

  • Clegg JS, Jackson SA (1989) Long term anoxia in Artemia cysts. J Exp Biol 147:539–543

    Google Scholar 

  • Clegg JS, Jackson SA (1998) The metabolic status of quiescent and diapause embryos of Artemia franciscana. Arch Hydrobiol 52:425–439

    Google Scholar 

  • Clegg JS, Trotman CAN (2002) Physiological and biochemical aspects of Artemia ecology. In: Abatzopoulos TJ, Beardmore JA, Clegg JS, Sorgeloos P (eds) Artemia: basic and applied biology. Kluwer Academic Publishers, Dordrecht, pp 129–170

    Google Scholar 

  • Clegg JS, Jackson SA, Warner AH (1994) Extensive intracellular translocations of a major protein accompany anoxia in embryos of Artemia franciscana. Exp Cell Res 212:77–83

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS, Jackson SA, Liang P, MacRae TH (1995) Nuclear-cytoplasmic translocations of protein p26 during aerobic-anoxic transitions in embryos of Artemia franciscana. Exp Cell Res 219:1–7

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS, Willsie JK, Jackson SA (1999) Adaptive significance of a small heat shock/alpha-crystallin protein (p26) in encysted embryos of the brine shrimp, Artemia franciscana. Am Zool 39:836–847

    CAS  Google Scholar 

  • Clegg JS, Jackson SA, Popov VI (2000a) Long term anoxia in encysted embryos of the crustacean, Artemia franciscana: viability, ultrastructure and stress proteins. Cell Tissue Res 301:433–446

    Article  PubMed  CAS  Google Scholar 

  • Clegg JS, Jackson SA, Hoa NV, Sorgeloos P (2000b) Thermal resistance, developmental rate and heat shock proteins in Artemia franciscana from San Francisco Bay and southern Vietnam. J Exp Mar Biol Ecol 252:85–96

    Article  PubMed  Google Scholar 

  • Cooper AF, Van Gundy SD (1970) Metabolism of glycogen and neutral lipids by Aphelenchus avenae and Caenorabditis sp. in aerobic, microaerobic and anaerobic environments. J Nematol 2:305–315

    PubMed  CAS  Google Scholar 

  • Crack JA, Mansour M, Sun Y, MacRae TH (2002) Functional analysis of a small heat shock/alpha-crystallin protein from Artemia franciscana: Oligomerization and thermotolerance. Eur J Biochem 269:1–10

    Article  Google Scholar 

  • Drinkwater LE, Clegg JS (1991) Experimental biology of cyst diapause. In: Browne RA, Sorgeloos P, Trotman CNA (eds) Artemia biology. CRC Press, Boca Raton, pp 93–118

    Google Scholar 

  • Dutrieu J, Chrestia-Blanchine D (1966) Résistance des oeufs durables hydratés d’Artemia salina à l’anoxie. CR Acad Sci Paris Série D 263:998–1000

    Google Scholar 

  • Ewing RD, Clegg JS (1969) Lactate dehydrogenase activity and anaerobic metabolism during the development of Artemia salina. Comp Biochem Physiol 31:297–307

    Article  PubMed  CAS  Google Scholar 

  • Guppy MG, Withers PC (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 7:1–40

    Google Scholar 

  • Hairston NG, Van Brunt RA, Kearns CM, Engstrom DR (1995) Age and survivorship of diapausing eggs in a sediment egg bank. Ecology 76:1706–1711

    Article  Google Scholar 

  • Hand SC (1998) Quiescence in Artemia franciscana embryos: reversible arrest of metabolism and gene expression at low oxygen levels. J Exp Biol 201:1233–1242

    PubMed  CAS  Google Scholar 

  • Hand SC, Gnaiger E (1988) Anaerobic dormancy quantified in Artemia embryos: a test of the control mechanism. Science 239:1425–1427

    Article  PubMed  CAS  Google Scholar 

  • Hand SC, Podrabsky JE (2000) Bioenergetics of diapause and quiescence in aquatic animals. Thermochim Acta 349:31–42

    Article  CAS  Google Scholar 

  • Hand SC, Jones D, Menze MA, Witt TL (2007) Life without water: expression of plant LEA genes by an anhydrobiotic arthropod. J Exp Zool Part A 307:62–66

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, New York

    Google Scholar 

  • Hontario R, Crowe JH, Crowe LE, Amat F (1993) Metabolic heat production by Artemia embryos. J Exp Biol 178:149–159

    Google Scholar 

  • Jackson SA, Clegg JS (1996) The ontogeny of low molecular weight stress protein p26 during early development of the brine shrimp, Artemia franciscana. Dev Growth Differ 38:153–160

    Article  CAS  Google Scholar 

  • Katajisto T (1996) Copepod eggs survive a decade in sediments of the Baltic Sea. Hydrobiologia 320:153–159

    Article  Google Scholar 

  • Katajisto T (2004) Effects of anoxia and hypoxia on the dormancy and survival of subitaneous eggs of Acartia bifilosa (Copepoda: Calanoida). Mar Biol 145:751–757

    Google Scholar 

  • Leopold AC (ed) (1986) Membranes, metabolism and dry organisms. Cornell University Press, Ithaca

    Google Scholar 

  • Liang P, MacRae TH (1999) The synthesis of a small heat shock/alpha-crystallin protein in Artemia and its relationship to stress tolerance during development. Dev Biol 207:445–456

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Amons R, MacRae TH, Clegg JS (1997a) Purification, structure and molecular chaperone activity in vitro of Artemia p26, a small heat shock/α-crystallin protein. Eur J Biochem 243:225–232

    Article  PubMed  CAS  Google Scholar 

  • Liang P, Amons R, Clegg JS, MacRae TH (1997b) Molecular characterization of a small heat-shock/α-crystallin protein from encysted Artemia embryos. J Biol Chem 272:19051–19058

    Article  PubMed  CAS  Google Scholar 

  • Liu L, Warner AH (2006) Further characterization of the cathepsin L-associated protein and its gene in two species of the brine shrimp. Artemia Comp Biochem Physiol A 145:458–467

    Article  Google Scholar 

  • MacRae TH (2003) Molecular chaperones, stress resistance and development in Artemia franciscana. Semin Cell Dev Biol 14:251–258

    Article  PubMed  CAS  Google Scholar 

  • MacRae TH (2005) Diapause: diverse states of developmental and metabolic arrest. J Biol Res 3:3–14

    CAS  Google Scholar 

  • MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424

    Article  PubMed  CAS  Google Scholar 

  • Marcus NH, Lutz R, Burnett W (1994) Age, viability and vertical distribution of zooplankton resting eggs from an anoxic basin: evidence of an egg bank. Limnol Oceanogr 39:154–158

    Article  Google Scholar 

  • McLennan AG (2009) Ametabolic embryos of Artemia franciscana accumulate DNA damage during prolonged anoxia. J Exp Biol 212:785–789

    Article  PubMed  CAS  Google Scholar 

  • Menze MA, Boswell L, Toner M, Hand SC (2009) Occurrence of mitochondria-targeted Late Embryogenesis Abundant (LEA) gene in animals increases organelle resistance to water stress. J Biol Chem 284:10714–10719

    Article  PubMed  CAS  Google Scholar 

  • Minsky A, Shimoni E, Frenkiel-Krispin D (2002) Stress, order and survival. Nat Rev 3:50–60

    Article  CAS  Google Scholar 

  • Muñoz J, Pacios F (2010) Global biodiversity and geographical distribution of diapausing aquatic invertebrates: the case of the cosmopolitan brine shrimp. Artemia (Branchiopoda, Anostraca) 83:465–480

    Google Scholar 

  • Nakanishi YH, Iwasaki T, Okigaki T, Kato H (1962) Cytological studies of Artemia salina. I. Embryonic development without cell multiplication after the blastula stage in encysted dry eggs. Annot Zool Jpn 35:223–228

    Google Scholar 

  • Nambu Z, Tanaka S, Nambu F, Nakano M (2008) Influence of temperature and darkness on embryonic diapause termination in dormant Artemia cysts that have never been desiccated. J Exp Zool A Ecol Genet Physiol 309:17–24

    PubMed  Google Scholar 

  • Nambu Z, Tanaka S, Nambu F, Nakano M (2009) Influence of darkness on embryonic diapause termination in dormant Artemia cysts with no experience of desiccation. J Exp Zool A Ecol Genet Physiol 311:182–188

    Article  PubMed  Google Scholar 

  • Olson C, Clegg JS (1978) Cell division during the development of Artemia salina. Wilhelm Roux’s Arch Entwickl Mech Org 184:1–13

    Article  Google Scholar 

  • Qiu Z, MacRae TH (2007) Developmentally regulated synthesis of p8, a stress-associated transcription cofactor, in diapause-destined embryos of Artemia franciscana. Cell Stress Chaperones 12:255–264

    Article  PubMed  CAS  Google Scholar 

  • Qiu Z, Macrae TH (2008a) ArHsp21, a developmentally regulated small heat-shock protein synthesized in diapausing embryos of Artemia franciscana. Biochem J 411:605–611

    Article  PubMed  CAS  Google Scholar 

  • Qiu Z, MacRae TH (2008b) ArHsp22, a developmentally regulated small heat shock protein produced in diapause-destined Artemia embryos, is stress inducible in adults. FEBS J 275:3556–3566

    Article  PubMed  CAS  Google Scholar 

  • Qiu Z, Bossier P, Wang X, Bojikova-Fournier S, MacRae TH (2006) Diversity, structure, and expression of the gene for p26, a small heat shock protein from Artemia. Genomics 88:230–240

    Article  PubMed  CAS  Google Scholar 

  • Robbins HM, Van Stappen G, Sorgeloos P, Sung YY, MacRae TH, Bossier P (2010) Diapause termination and development of encysted Artemia embryos: roles for nitric oxide and hydrogen peroxide. J Exp Biol 213:1464–1470

    Article  PubMed  CAS  Google Scholar 

  • Sharon MA, Kozarova A, Clegg JS, Vacratsis PO, Warner AH (2009) Characterization of a group 1 late embryogenesis abundant protein in encysted embryos of the brine shrimp Artemia franciscana. Biochem Cell Biol 87:415–430

    Article  PubMed  CAS  Google Scholar 

  • Stocco DM, Beers PC, Warner AH (1972) Effects of anoxia on nucleotide metabolism in encysted embryos of the brine shrimp. Dev Biol 27:479–493

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476

    Article  PubMed  CAS  Google Scholar 

  • Tanguay JA, Reyes RC, Clegg JS (2004) Habitat diversity and adaptation to environmental stress in encysted embryos of the crustacean Artemia. J Biosci 29:489–501

    Article  PubMed  Google Scholar 

  • Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812

    Article  PubMed  CAS  Google Scholar 

  • Tunnacliffe A, Hincha DK, Leprince O (2010) LEA proteins: versatility of form and function. In: Lubzens E, Cerda I, Clark M (eds) Dormancy and resistance in harsh environments. Springer, Berlin, pp 91–108

    Chapter  Google Scholar 

  • Viner RI, Clegg JS (2001) Influence of trehalose on the molecular chaperone activity of p26, a small heat shock protein. Cell Stress Chaperones 6:126–135

    Article  PubMed  CAS  Google Scholar 

  • Warner AH, Clegg JS (2001) Diguanosine nucleotide metabolism and the survival of Artemia embryos during years of continuous anoxia. Eur J Biochem 268:1569–1576

    Article  Google Scholar 

  • Warner AH, Jackson SA, Clegg JS (1997) Effect of anaerobiosis on cysteine protease regulation during the embryonic-larval transition in Artemia franciscana. J Exp Biol 200:897–908

    PubMed  CAS  Google Scholar 

  • Warner AH, Brunet RT, MacRae TH, Clegg JS (2004) Artemin is an RNA-binding protein with high thermal stability and potential RNA chaperone activity. Arch Biochem Biophys 424:189–200

    Article  PubMed  CAS  Google Scholar 

  • Wharton DA (2002) Survival strategies. In: Lee DL (ed) The biology of nematodes. Taylor & Francis, London, pp 389–411

    Google Scholar 

  • Willsie JK, Clegg JS (2001) Nuclear p26, a small heat shock protein, and its relationship to stress resistance in Artemia franciscana embryos. J Exp Biol 204:2339–2350

    PubMed  CAS  Google Scholar 

  • Willsie JK, Clegg JS (2002) Small heat shock protein p26 associates with nuclear lamins and HSP70 in nuclei and nuclear matrix fractions from stressed cells. J Cell Biochem 84:601–614

    Article  PubMed  Google Scholar 

  • Withers PC, Cooper CE (2010) Metabolic depression: a historical perspective. In: Navas CA, Carvalho JE (eds) Aestivation. Molecular and physiological aspects. Springer, Berlin, pp 1–24

    Google Scholar 

Download references

Acknowledgments

Long time collaborations with Professors Tom MacRae and Al Warner, and members of their laboratories, have been very valuable as we all attempt to understand the remarkable animal extremophile, Artemia. Partially supported by CRIS project Ca-D*-BML-5207-H, Ag. Exp. Station, University of California.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James S. Clegg .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer Science+Business Media B.V.

About this chapter

Cite this chapter

Clegg, J.S. (2012). The Unusual Response of Encysted Embryos of the Animal Extremophile, Artemia franciscana, to Prolonged Anoxia. In: Altenbach, A., Bernhard, J., Seckbach, J. (eds) Anoxia. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 21. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1896-8_11

Download citation

Publish with us

Policies and ethics