Tolerance of resting cells of freshwater and terrestrial benthic diatoms to experimental desiccation and freezing is habitat-dependent

REFERENCES

• Alve E. & Goldstein S.T. 2010. Dispersal, survival and delayed growth of benthic foraminiferal propagules. Journal of Sea Research 63: 36–51.
   Web of Science ®Google Scholar
• Anderson O.R. 1975. Ultrastructure and cytochemistry of resting cell formation in Amphora coffeaeformis (Bacillariophyceae). Journal of Phycology 11: 272–281.
   Web of Science ®Google Scholar
• Anderson O.R. 2010. Field and laboratory studies of encysted and trophic stages of naked amoebae, including a perspective on population life cycle dynamics. Acta Protozoologica 49: 1–8.
   Web of Science ®Google Scholar
• Baker P.D. & Bellifemine D. 2000. Environmental influences on akinete germination of Anabaena circinalis and implications for management of cyanobacterial blooms. Hydrobiologia 427: 65–73.
   Web of Science ®Google Scholar
• Bayley M., Petersen S.O., Knigge T., Kohler H.R. & Holmstrup M. 2001. Drought acclimation confers cold tolerance in the soil collembolan Folsomia candida. Journal of Insect Physiology 47: 1197–1204.
   Web of Science ®Google Scholar
• Bierkens J., Van De Perre W. & Maes J. 1998. Effect of different environmental variables on the synthesis of Hsp70 in Raphidocelis subcapitata. Comparative Biochemistry and Physiology. Part A. Molecular and Integrative Physiology 120: 29–34.
   Web of Science ®Google Scholar
• Brown R.M., Larson D.A. & Bold H.C. 1964. Airborne algae - their abundance and heterogeneity. Science 143: 583.
   PubMed Web of Science ®Google Scholar
• Bushnell J.H. & Rao K.S. 1974. Dormant or quiescent stages and structures among Ectoprocta. Physical and chemical factors affecting viability and germination of statoblasts. Transactions of the American Microscopical Society 93: 524–543.
   Google Scholar
• Butterwick C., Heaney S.I. & Talling J.F. 2005. Diversity in the influence of temperature on the growth rates of freshwater algae, and its ecological relevance. Freshwater Biology 50: 291–300.
   Web of Science ®Google Scholar
• Consalvey M., Perkins R.G., Paterson D.M. & Underwood G.J.C. 2005. PAM fluorescence: A beginners guide for benthic diatomists. Diatom Research 20: 1–22.
   Web of Science ®Google Scholar
• Crowe J.H., Carpenter J.F., Crowe L.M. & Anchordoguy T.J. 1990. Are freezing and dehydration similar stress vectors? A comparison of modes of interaction of stabilizing solutes with biomolecules. Cryobiology 27: 219–231.
   Web of Science ®Google Scholar
• Dring M.J. 2006. Stress resistance and disease resistance in seaweeds: The role of reactive oxygen metabolism. In: Advances in botanical research, Vol 43. Incorporating advances in plant pathology. (Ed. by J.A. Callow), pp. 175–207. Academic Press Ltd-Elsevier science Ltd, London.
   Google Scholar
• Dunlap C.A., Evans K.O., Theelen B., Boekhout T. & Schisler D.A. 2007. Osmotic shock tolerance and membrane fluidity of cold-adapted Cryptococcus flavescens OH 182.9, previously reported as C. nodaensis, a biocontrol agent of Fusarium head blight. Fems Yeast Research 7: 449–458.
   Web of Science ®Google Scholar
• Elster J., Degma P., Kovacik L., Valentova L., Sramkova K. & Pereira A.B. 2008. Freezing and desiccation injury resistance in the filamentous green alga Klebsormidium from the Antarctic, Arctic and Slovakia. Biologia 63: 843–851.
   Web of Science ®Google Scholar
• Ettl H. & Gärtner G. 1995. Syllabus der Boden-, Luft-und Flechtenalgen. Gustav Fisher Verlag, Stuttgart. 721 pp.
   Google Scholar
• Evans J.H. 1958. The survival of freshwater algae during dry periods. 1. An investigation of the algae of 5 small ponds. Journal of Ecology 46: 149–167.
   Web of Science ®Google Scholar
• Evans J.H. 1959. The survival of freshwater algae during dry periods. 2. Drying experiments. 3. Stratification of algae in pond margin litter and mud. Journal of Ecology 47: 55–81.
   Web of Science ®Google Scholar
• Evans K.M., Chepurnov V.A., Sluiman H.J., Thomas S.J., Spears B.M. & Mann D.G. 2009. Highly differentiated populations of the freshwater diatom Sellaphora capitata suggest limited dispersal and opportunities for allopatric speciation. Protist 160: 386–396.
   PubMed Web of Science ®Google Scholar
• Figuerola J., Green A.J. & Michot T.C. 2005. Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. American Naturalist 165: 274–280.
   PubMed Web of Science ®Google Scholar
• Fryer G. 1996. Diapause, a potent force in the evolution of freshwater crustaceans. Hydrobiologia 320: 1–14.
   Web of Science ®Google Scholar
• Gao Z., Horton R., Wang L., Liu H. & Wen J. 2008. An improved force-restore method for soil temperature prediction. European Journal of Soil Science 59: 972–981.
   Web of Science ®Google Scholar
• Gilbert J.J. & Schreiber D.K. 1995. Induction of diapausing amictic eggs in Synchaeta pectinata. Hydrobiologia 313: 345–350.
   Web of Science ®Google Scholar
• Gran H.H. 1912. Pelagic plant life. In: The depths of the ocean. (Ed. by J. Murray & J. Hjort), pp. 307–386. Macmillan, London.
   Google Scholar
• Gray D.W., Lewis L.A. & Cardon Z.G. 2007. Photosynthetic recovery following desiccation of desert green algae (Chlorophyta) and their aquatic relatives. Plant Cell and Environment 30: 1240–1255.
   PubMed Web of Science ®Google Scholar
• Guillard R.R.L. & Lorenzen C.L. 1972. Yellow-green algae with chlorophyllide c. Journal of Phycology 4: 59–64.
   Google Scholar
• Gupta S. & Agrawal S.C. 2006. Survival of blue-green and green algae under stress conditions. Folia Microbiologica 51: 121–128.
   PubMed Web of Science ®Google Scholar
• Hargraves P.E. & French F.W. 1975. Observations on the survival of diatoms resting spores. Nova Hedwigia Beihefte 53: 229–238.
   Google Scholar
• Hargraves P.E. & French F.W. 1983. Diatom resting spores: significance and strategies. In: Survival strategies of the algae. (Ed. by G.A. Fryxell), pp. 49–68. Cambridge University Press, New York.
   Google Scholar
• Härnström K., Ellegaard M., Andersen T.J. & Godhe A. 2011. Hundred years of genetic structure in a sediment revived diatom population. Proceedings of the National Academy of Sciences of the United States of America 108: 4252–4257.
   PubMed Web of Science ®Google Scholar
• Hayward S.A.L., Rinehart J.P., Sandro L.H., Lee R.E. & Denlinger D.L. 2007. Slow dehydration promotes desiccation and freeze tolerance in the Antarctic midge Belgica antarctica. Journal of Experimental Biology 210: 836–844.
   Web of Science ®Google Scholar
• Hollibaugh J.T., Seibert D.L.R. & Thomas W.H. 1981. Observations on the survival and germination of resting spores of three Chaetoceros (Bacillariophyceae) species. Journal of Phycology 17: 1–9.
   Web of Science ®Google Scholar
• Hori K., Okamoto J., Tanji Y. & Unno H. 2003. Formation, sedimentation and germination properties of Anabaena akinetes. Biochemical Engineering Journal 14: 67–73.
   Web of Science ®Google Scholar
• Hostetter H.P. & Hoshaw R.W. 1970. Environmental factors affecting resistance to desiccation in the diatom Stauroneis anceps. American Journal of Botany 57: 512–518.
   Web of Science ®Google Scholar
• Isard S.A. & Gage S.H. 2001. Flow of life in the atmosphere: an airscape approach to understanding invasive organisms. Michigan state University Press, East Lansing. 304 pp.
   Google Scholar
• Jaworski G.J. & Lund J.W.G. 1970. Drought resistance and dispersal of Asterionella formosa Hass. Nova Hedwigia Beihefte 31: 37–48.
   Google Scholar
• Jewson D.H., Lowry S.F. & Bowen R. 2006. Co-existence and survival of diatoms on sand grains. European Journal of Phycology 41: 131–146.
   Web of Science ®Google Scholar
• Johansen J.R. 1999. Chapter 12. Diatoms of aerial habitats. In: The diatoms: applications for the environmental and earth sciences. (Ed. by E.F. Stoermer & J.P. Smol), pp. 264–273. Cambridge University Press, Cambridge, UK.
   Google Scholar
• Krammer K. & Lange-Bertalot H. 1988. Bacillariophyceae 2, Teil. Epithemiaceae, Bacillariaceae, Surillellaceae. Gustav Fisher Verlag, stuttgart. 596 pp.
   Google Scholar
• Krammer K. & Lange-Bertalot H. 1991. Bacillariophyceae 4, Teil. Achnanthaceae. Kritische Ergänzungenzu Navicula (Lineolata) und Gomphonema. Gustav Fisher Verlag, Stuttgart. 436 pp.
   Google Scholar
• Kristiansen J. 1996. Dispersal of freshwater algae - a review. Hydrobiologia 336: 151–157.
   Web of Science ®Google Scholar
• Kuwata A. & Takahashi M. 1990. Life-form population responses of a marine planktonic diatom, Chaetoceros pseudocurvisetus, to oligothophication in regionally upwelled water. Marine Biology 107: 503–512.
   Web of Science ®Google Scholar
• Kuwata A., Hama T. & Takahashi M. 1993. Ecophysiological characterization of two life forms, resting spores and resting cells, of a marine phytoplanktonic diatom, Chaetoceros pseudocurvisetus, formed under nitrogen depletion. Marine Ecology-Progress Series 102: 245–255.
   Web of Science ®Google Scholar
• Lund J.W.G. 1953. The seasonal cycle of the plankton diatom Melosira italica (Ehr.) Kutz. subsp. subarctica o. Mull. Journal of Ecology 42: 151–179.
   Web of Science ®Google Scholar
• Mann D.G. & Evans K.M. 2007. Molecular genetics and the neglected art of diatomics. In: Unraveling the algae — the past, present and future of alga molecular systematics. (Ed. by J. Brodie & J.M. Lewis), pp. 321–265. CRC Press, London.
   Google Scholar
• Mcquoid M.R. & Hobson L.A. 1995. Importance of resting stages in diatom seasonal succession. Journal of Phycology 31: 44–50.
   Web of Science ®Google Scholar
• Mcquoid M.R. & Hobson L.A. 1996. Diatom resting stages. Journal of Phycology 32: 889–902.
   Web of Science ®Google Scholar
• Müller H., Achilles-Day U.E.M. & Day J.G. 2010. Tolerance of the resting cysts of Colpoda inflata (Ciliophora, Colpodea) and Meseres corlissi (Ciliophora, Spirotrichea) to desiccation and freezing. European Journal of Protistology 46: 133–142.
   Web of Science ®Google Scholar
• Nicholson W.L., Munakata N., Horneck G., Melosh H.J. & Setlow P. 2000. Resistance of Bacillus endospores to extreme terrestrial and extraterrestrial environments. Microbiology and Molecular Biology Reviews 64: 548–572.
   PubMed Web of Science ®Google Scholar
• Oldenhof H., Wolkers W.F., Bowman J.L., Tablin F. & Crowe J.H. 2006. Freezing and desiccation tolerance in the moss Physcomitrella patens: An in situ Fourier transform infrared spectroscopic study. Biochimica Et Biophysica Acta-General Subjects 1760: 1226–1234.
   PubMed Web of Science ®Google Scholar
• Perkins R.G., Lavaud J., Serodio J., Mouget J.L., Cartaxana P., Rosa P., Barille L., Brotas V. & Jesus B.M. 2010. Vertical cell movement is a primary response of intertidal benthic biofilms to increasing light dose. Marine Ecology-Progress Series 416: 93–103.
   Web of Science ®Google Scholar
• Persson A. 2002. Proliferation of cryptic protists and germination of resting stages from untreated sediment samples with emphasis on dinoflagellates. Ophelia 55: 151–166.
   Google Scholar
• Petersen J.B. 1935. Studies on the biology and taxonomy of soil algae. Dansk Botanisk Arkiv 8: 1–180.
   Google Scholar
• Potts M. 1999. Mechanisms of desiccation tolerance in cyanobacteria. European Journal of Phycology 34: 319–328.
   Web of Science ®Google Scholar
• Poulickova A., Lysakova M., Hasler P. & Lelkova E. 2008. Fishpond sediments - the source of palaeoecological information and algal “seed banks”. Nova Hedwigia 86: 141–153.
   Web of Science ®Google Scholar
• Rajendran U.M., Kathirvel E. & Anand N. 2007. Desiccation-induced changes in antioxidant enzymes, fatty acids, and amino acids in the cyanobacterium Tolypothrix scytonemoides. World Journal of Microbiology & Biotechnology 23: 251–257.
   Web of Science ®Google Scholar
• Rengefors K. & Anderson D.M. 1998. Environmental and endogenous regulation of cyst germination in two freshwater dinoflagellates. Journal of Phycology 34: 568–577.
   Web of Science ®Google Scholar
• Round F.E., Crawford R.M. & Mann D.G. 1990. The diatoms: biology and morphology of the genera. Cambridge University Press, Cambridge, UK. 747 pp.
   Google Scholar
• Rousch J.M., Bingham S.E. & Sommerfeld M.R. 2003. Changes in fatty acid profiles of thermo-intolerant and thermo-tolerant marine diatoms during temperature stress. Journal of Experimental Marine Biology and Ecology 295: 145–156.
   Web of Science ®Google Scholar
• Rousch J.M., Bingham S.E. & Sommerfeld M.R. 2004. Protein expression during heat stress in thermo-intolerant and thermo-tolerant diatoms. Journal of Experimental Marine Biology and Ecology 306: 231–243.
   Web of Science ®Google Scholar
• Roy-Ocotla G. & Carrera J. 1993. Aeroalgae - responses to some aerobiological questions. Grana 32: 48–56.
   Web of Science ®Google Scholar
• Sabacka M. & Elster J. 2006. Response of cyanobacteria and algae from Antarctic wetland habitats to freezing and desiccation stress. Polar Biology 30: 31–37.
   Web of Science ®Google Scholar
• Sarno D., Kooistra W., Medlin L.K., Percopo I. & Zingone A. 2005. Diversity in the genus Skeletonema (Bacillariophyceae). II. An assessment of the taxonomy of S. costatum-like species with the description of four new species. Journal of Phycology 41: 151–176.
   Web of Science ®Google Scholar
• Schelske C.L., Carrick H.J. & Aldridge F.J. 1995. Can wind-induced resuspension of meroplankton affect phytoplankton dynamics? Journal of the North American Benthological Society 14: 616–630.
   Web of Science ®Google Scholar
• Schlichting H.E. 1961. Viable species of algae and protozoa in the atmosphere. Lloydia 24: 81–88.
   Google Scholar
• Schlichting H.E. 1964. Meteorological conditions affecting dipsersal of airborne algae + protozoa. Lloydia 27: 64.
   Google Scholar
• Schmid A.M.M. 2009. Induction of resting-spores in the pennate diatom Navicula (Craticula) cuspidata by uncoupling of the cell and plastid cycles. Nova Hedwigia: 85–101.
   Google Scholar
• Scholnik D.A. 1994. Seasonal variation and diurnal fluctuation in ephemeral desert pools. Hydrobiologia 294: 111–116.
   Web of Science ®Google Scholar
• Sicko-Goad L., Stoermer E.F. & Fahnenstiel G. 1986. Rejuvenation of Melosira granulata (Bacillariophyceae) resting cells from the anoxic sediments of Douglas lake, Michigan. I. Light microscopy and C-14 uptake. Journal of Phycology 22: 22–28.
   Web of Science ®Google Scholar
• Sicko-Goad L., Stoermer E.F. & Kociolek J.P. 1989. Diatom resting cell rejuvenation and formation - time course, species records and distribution. Journal of Plankton Research 11: 375–389.
   Web of Science ®Google Scholar
• Slobodkin L.B. 1954. Population dynamics in Daphnia obtusa Kurz. Ecological Monographs 24: 69–88.
   Web of Science ®Google Scholar
• Smirnoff N. 1993. The role of active oxygen in the response of plants to water-deficit and desiccation. New Phytologist 125: 27–58.
   PubMed Web of Science ®Google Scholar
• Souffreau C., Vanormelingen P., Verleyen E., Sabbe K. & Vyverman W. 2010. Tolerance of benthic diatoms from temperate aquatic and terrestrial habitats to experimental desiccation and temperature stress. Phycologia 49: 309–324.
   Web of Science ®Google Scholar
• Souffreau C., Verbruggen H., Wolfe A.P., Vanormelingen P., Siver P.A., Cox E.J., Mann D.G., Van De Vijver B., Sabbe K. & Vyverman W. 2011. A time-calibrated multi-gene phylogeny of the diatom genus Pinnularia. Molecular Phylogenetics and Evolution 61: 866–879.
   PubMed Web of Science ®Google Scholar
• Souffreau C., Vanormelingen P., Van De Vijver B., Isheva T., Verleyen E., Sabbe K. & Vyverman W. 2013. Molecular evidence for distinct Antarctic lineages in the cosmopolitan terrestrial diatoms Pinnularia borealis and Hantzschia amphioxys. Protist 164: 101–115.
   PubMed Web of Science ®Google Scholar
• Spaulding S.A., Van De Vijver B., Hodgson A., Mcknight D.M., Verleyen E. & Stanish L. 2010. Diatoms as indicators of environmental change in Antarctic and subantarctic fresh waters. In: The diatoms: applications for the environmental and earth sciences. (Ed. by J.P. Smol & E.F. Stoermer), pp. 267–283. Cambridge University Press, Cambridge, UK.
   Google Scholar
• Starks T.L., Shubert L.E. & Trainor F.R. 1981. Ecology of soil algae - a review. Phycologia 20: 65–80.
   Web of Science ®Google Scholar
• Sung D.Y., Kaplan F., Lee K.J. & Guy C.L. 2003. Acquired tolerance to temperature extremes. Trends in Plant Science 8: 179–187.
   PubMed Web of Science ®Google Scholar
• Sutherland J.M., Herdman M. & Stewart W.D.P. 1979. Akinetes of the cyanobacterium Nostoc-Pcc-7524. Macromolecular composition, structure and control of differentiation. Journal of General Microbiology 115: 273–287.
   Google Scholar
• Tamaru Y., Takani Y., Yoshida T. & Sakamoto T. 2005. Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Applied and Environmental Microbiology 71: 7327–7333.
   PubMed Web of Science ®Google Scholar
• Templeton A.R. 2008. The reality and importance of founder speciation in evolution. Bioessays 30: 470–479.
   Web of Science ®Google Scholar
• Trobajo R., Mann D.G., Chepurnov V.A., Clavero E. & Cox E.J. 2006. Taxonomy, life cycle, and auxosporulation of Nitzschia fonticola (Bacillariophyta). Journal of Phycology 42: 1353–1372.
   Web of Science ®Google Scholar
• Trobajo R., Clavero E., Chepurnov V.A., Sabbe K., Mann D.G., Ishihara S. & Cox E.J. 2009. Morphological, genetic and mating diversity within the widespread bioindicator Nitzschia palea (Bacillariophyceae). Phycologia 48: 443–459.
   Web of Science ®Google Scholar
• Van Dam H., Mertens A. & Sinkeldam J. 1994. A coded checklist and ecological indicator values of freshwater diatoms from the Netherlands. Netherlands Journal of Aquatic Ecology 28: 117–133.
   Google Scholar
• Van de Vijver B., Beyens L., Vincke S. & Gremmen N.J.M. 2004. Moss-inhabiting diatom communities from Heard Island, sub-Antarctic. Polar Biology 27: 532–543.
   Web of Science ®Google Scholar
• Van Kerckvoorde A., Trappeniers K., Nijs I. & Beyens L. 2000. Terrestrial soil diatom assemblages from different vegetation types in Zackenberg (Northeast Greenland). Polar Biology 23: 392–400.
   Web of Science ®Google Scholar
• Van Overeem M.A. 1937. On green organisms occuring in the lower troposhere. Recueil des Travaux Botanique Neerlandais 34: 388–442.
   Google Scholar
• Vanelslander B., Creach V., Vanormelingen P., Ernst A., Chepurnov V.A., Sahan E., Muyzer G., Stal L.J., Vyverman W. & Sabbe K. 2009. Ecological differentiation between sympatric pseudocryptic species in the estuarine benthic diatom Navicula phyllepta (Bacillariophyceae). Journal of Phycology 45: 1278–1289.
   PubMed Web of Science ®Google Scholar
• Vanormelingen P., Chepurnov V.A., Mann D.G., Sabbe K. & Vyverman W. 2008. Genetic divergence and reproductive barriers among morphologically heterogeneous sympatric clones of Eunotia bilunaris sensu lato (Bacillariophyta). Protist 159: 73–90.
   PubMed Web of Science ®Google Scholar
• Villanueva V.D. 2006. Diatom distribution in a temporary pond from the Patagonian Andes (Fantasma Pond) during drought. Nova Hedwigia 83: 459–472.
   Web of Science ®Google Scholar
• Welsh D.T. 2000. Ecological significance of compatible solute accumulation by micro-organisms: from single cells to global climate. FEMS Microbiology Reviews 24: 263–290.
   PubMed Web of Science ®Google Scholar