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Microbial Eukaryotes in Hypersaline Anoxic Deep-Sea Basins

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Polyextremophiles

Part of the book series: Cellular Origin, Life in Extreme Habitats and Astrobiology ((COLE,volume 27))

Abstract

The combination of high hydrostatic pressure, absence of light, anoxia, nearly saturated salt concentration and corresponding high density, and a sharp chemocline makes the deep hypersaline anoxic basins in the Eastern Mediterranean Sea some of the most polyextreme habitats on Earth. Once considered anathema to life, deep hypersaline anoxic basins (DHABs) are now known to host diverse microbial life, including eukaryotes. The haloclines and brines of DHABs with different chemistries appear to host distinct populations of microbiota. The most abundant groups of eukaryotes detected by small subunit ribosomal RNA-based molecular analyses and microscopy to date are members of the alveolates, kinetoplastids, and fungi. While the specific adaptations that allow these taxa to survive under such polyextreme condition are still unknown, many ciliates in halocline water samples have been observed to host bacterial and/or archaeal epibiotic partners. Symbiosis may represent one strategy enabling eukaryotic survival in DHAB environments.

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References

  • Alexander E, Stock A, Breiner HW, Behnke A, Bunge J, Yakimov MM, Stoeck T (2009) Microbial eukaryotes in the hypersaline anoxic L’Atalante deep-sea basin. Environ Microbiol 11:360–381

    Article  PubMed  CAS  Google Scholar 

  • Barry JP, Greene HG, Orange DL, Baxter CH, Robinson BH, Kochevar RE, Nybakken JW, Reed DL, McHugh CM (1996) Biologic and geologic characteristics of cold seeps in Monterey Bay, California. Deep-Sea Res 43:1739–1762

    Article  CAS  Google Scholar 

  • Bernhard JM, Sen Gupta BK (1999) Foraminifera of oxygen-depleted environments. In: Sen Gupta BK (ed) Modern Foraminifera. Kluwer Academic, Dordrecht, pp 201–216

    Google Scholar 

  • Bernhard JM, Buck KR, Farmer MA, Bowser SS (2000) The Santa Barbara Basin is a symbiosis oasis. Nature 403:77–80

    Article  PubMed  CAS  Google Scholar 

  • Borin S, Brusetti L, Mapelli F, D’Auria G, Brusa T, Marzorati M, Rizzi A, Yakimov M, Marty D, De Lange GJ, van der Wielen P, Bolhuis H, McGenity TJ, Polymenakou PN, Malinverno E, Giuliano L, Corselli C, Daffonchio D (2009) Sulfur cycling and methanogenesis primarily drive microbial colonization of the highly sulfidic Urania deep hypersaline basin. Proc Natl Acad Sci USA 106:9151–9156

    Article  PubMed  CAS  Google Scholar 

  • Cavanaugh CM (1994) Microbial symbiosis: patterns of diversity in the marine environment. Am Zool 34:79–89

    Google Scholar 

  • Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW, Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science 213:340–341

    Article  PubMed  CAS  Google Scholar 

  • Cita MB (2006) Exhumation of Messinian evaporites in the deep-sea and creation of deep anoxic brine filled collapsed basins. Sed Geol 188–189:357–378

    Article  Google Scholar 

  • Daffonchio D, Borin S, Brusa T, Brusetti L, van der Wielen PW, Bolhuis H, Yakimov MM, D’Auria G, Giuliano L, Marty D, Tamburini C, McGenity TJ, Hallsworth JE, Sass AM, Timmis KN, Tselepides A, de Lange GJ, Hubner A, Thomson J, Varnavas SP, Gasparoni F, Gerber HW, Malinverno E, Corselli C, Garcin J, McKew B, Golyshin PN, Lampadariou N, Polymenakou P, Calore D, Cenedese S, Zanon F, Hoog S (2006) Stratified prokaryote network in the oxic-anoxic transition of a deep-sea halocline. Nature 440:203–207

    Article  PubMed  CAS  Google Scholar 

  • Danovaro R, Dell’Anno A, Pusceddu A, Gambi C, Heiner I, Kristensen RM (2010) The first metazoa living in permanently anoxic conditions. BMC Biol 8:30. doi:10.1186/1741-7007-8-30

    Article  PubMed  Google Scholar 

  • Distel DL, Felbeck H (1988) Pathways of inorganic carbon fixation in the endosymbiont-bearing lucinid clam Lucinoma aequizonata. I. Purification and characterization of endosymbiotic bacteria. J Exp Zool 247:1–10

    Article  CAS  Google Scholar 

  • Eder W, Ludwig W, Huber R (1999) Novel 16S rRNA gene sequences retrieved from highly saline brine sediments of kebrit deep, red Sea. Arch Microbiol 172:213–218

    Article  PubMed  CAS  Google Scholar 

  • Eder W, Jahnke LL, Schmidt M, Huber R (2001) Microbial diversity of the brine-seawater interface of the Kebrit Deep, Red Sea, studied via 16S rRNA gene sequences and cultivation methods. Appl Environ Microbiol 67:3077–3085

    Article  PubMed  CAS  Google Scholar 

  • Eder W, Schmidt M, Koch M, Garbe-Schonberg D, Huber R (2002) Prokaryotic phylogenetic diversity and corresponding geochemical data of the brine-seawater interface of the Shaban Deep, Red Sea. Environ Microbiol 4:758–763

    Article  PubMed  CAS  Google Scholar 

  • Edgcomb V, Orsi W, Leslin C, Epstein SS, Bunge J, Jeon S, Yakimov MM, Behnke A, Stoeck T (2009) Protistan community patterns within the brine and halocline of deep hypersaline anoxic basins in the eastern Mediterranean Sea. Extremophiles 13:151–167

    Article  PubMed  Google Scholar 

  • Edgcomb V, Breglia SA, Yubuki N, Beaudoin D, Patterson DJ, Leander BS, Bernhard JM (2010) Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution. ISME J 5:11–13

    Google Scholar 

  • Edgcomb V, Orsi W, Bunge J, Jeon SO, Christen R, Leslin C, Holder M, Taylor GT, Suarez P, Varela R, Epstein S (2011a) Protistan microbial observatory in the Cariaco Basin, Caribbean. I. Pyrosequencing vs. Sanger insights into species richness. ISME J 5:1344–1356

    Article  PubMed  CAS  Google Scholar 

  • Edgcomb VP, Orsi W, Breiner H-W, Stock A, Filker S, Yakimov MM, Stoeck T (2011b) Novel kinetoplastids associated with hypersaline anoxic lakes in the Eastern Mediterranean deep-sea. Deep-Sea Res 58:1040–1048

    Article  CAS  Google Scholar 

  • Edgcomb VP, Orsi W, Taylor GT, Vdacny P, Taylor C, Suarez P, Epstein S (2011c) Accessing marine protists from the anoxic Cariaco Basin. ISME J 5:1237–1241

    Article  PubMed  CAS  Google Scholar 

  • Elloumi J, Carrias J-F, Ayadi H, Sime-Ngando T, Boukhris M, Bouain A (2006) Composition and distribution of planktonic ciliates from ponds of different salinity in the solar saltwork of Sfax. Tunisia Estuar Coast Shelf Sci 67:21–29

    Article  Google Scholar 

  • Embley TM, Finlay BJ (1993) Systematic and morphological diversity of endosymbiotic methanogens in anaerobic ciliates. Antonie van Leeuwenhoek 64:261–271

    Article  PubMed  Google Scholar 

  • Embley TM, Finlay BJ (1994) The use of small subunit rRNA sequences to unravel the relationships between anaerobic ciliates and their methanogen endosymbionts. Microbiology 140:225–235

    Article  PubMed  CAS  Google Scholar 

  • Fenchel T, Finlay BJ (1991) The biology of free-living anaerobic ciliates. Eur J Protistol 26:201–215

    Article  PubMed  CAS  Google Scholar 

  • Finlay BJ (1990) Physiological ecology of free-living protozoa. Adv Microbiol Ecol 11:1–34

    Article  CAS  Google Scholar 

  • Hallsworth JE, Yakimov MM, Golyshin PN, Gillion JL, D’Auria G, de Lima Alves F, La Cono V, Genovese M, McKew BA, Hayes SL, Harris G, Giuliano L, Timmis KN, McGenity TJ (2007) Limits of life in MgCl2-containing environments: chaotropicity defines the window. Environ Microbiol 9:801–813

    Article  PubMed  CAS  Google Scholar 

  • Hauer G, Rogerson A (2005) Heterotrophic protozoa from hypersaline environments. In: Gunde-Cimerman N, Oren A, PlemenitaÅ¡ A (eds) Adaptation to life at high salt concentrations in archaea, bacteria, and eukarya. Springer, Dordrecht, pp 519–540

    Chapter  Google Scholar 

  • Hickman C (2005) The influence of cooperative bacteria on animal host biology. In: McFall-Ngai MJ, Henderson B, Ruby EG (eds) Advances in molecular and cellular microbiology. Cambridge Press, Cambridge, 61 pp

    Google Scholar 

  • Nowack EC, Melkonin M (2010) Endosymbiotic associations within protists. Philos Trans R Soc 365:699–712

    Article  CAS  Google Scholar 

  • Oren A (2000) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Indust Microbiol Biotechnol 28:56–63

    Google Scholar 

  • Orsi W, Charvet S, Bernhard J, Edgcomb VP (2012) Prevalence of partnerships between bacteria and ciliates in oxygen-depleted marine water columns. Front Ext Microbiol 3:341

    Google Scholar 

  • Pedros-Alió C, Calderón-Paz JI, MacLean MH, Medina G, Marrasé C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155

    Article  PubMed  Google Scholar 

  • Por F (1980) A classification of hypersaline waters, based on trophic criteria. Mar Ecol 1:121–131

    Article  Google Scholar 

  • Ramos-Cormenzana A (1991) Halophilic organisms and their environment. In: Rodriguez-Valera F (ed) General and applied aspects of halophilic microorganisms. Plenum Press, New York, pp 15–24

    Chapter  Google Scholar 

  • Sass AM, Sass H, Coolen MJ, Cypionka H, Overmann J (2001) Microbial communities in the chemocline of a hypersaline deep-sea basin (Urania basin, Mediterranean Sea). Appl Environ Microbiol 67:5392–5402

    Article  PubMed  CAS  Google Scholar 

  • Stock A, Breiner H-W, Pachiadaki M, Edgcomb V, Filker S, LaCono V, Yakimov MM, Stoeck T (2011) Microbial eukaryote life in the new hypersaline deep-sea basin Thetis. Extremophiles 16:21–34

    Article  PubMed  Google Scholar 

  • Stoeck T, Fowle WH, Epstein SS (2003) Methodology of protistan discovery: from rRNA detection to quality scanning electron microscope images. Appl Environ Microbiol 69:6856–6863

    Article  PubMed  CAS  Google Scholar 

  • Stoeck T, Hayward B, Taylor GT, Varela R, Epstein SS (2006) A multiple PCR-primer approach to access the microeukaryotic diversity in environmental samples. Protist 157:31–43

    Article  PubMed  CAS  Google Scholar 

  • Taylor GT, Scranton ML, Iabichella M, Ho T-Y, Thunell RC, Muller-Karger F, Varela R (2001) Chemoautotrophy in the redox transition zone of the Cariaco Basin: a significant midwater source of organic carbon production. Limnol Oceanogr 46:148–163

    Article  CAS  Google Scholar 

  • Taylor GT, Iabichella-Armas M, Varela R, Müller-Karger F, Lin X, Scranton ML (2006) Microbial ecology of the Cariaco basin’s redoxcline. In: Neretin NL (ed) Past and present water column anoxia. Springer, Dordrecht, pp 473–499

    Google Scholar 

  • Tribovillard N, Bout-Roumazeilles V, Algeo T, Lyons TW, Sionneau T, Montero-Serrano JC, Riboulleau A, Baudin F (2008) Paleodepositional conditions in the Orca Basin as inferred from organic matter and trace metal contents. Mar Geol 254:62–72

    Article  CAS  Google Scholar 

  • van der Wielen PW, Heijs SK (2007) Sulfate-reducing prokaryotic communities in two deep hypersaline anoxic basins in the Eastern Mediterranean deep sea. Environ Microbiol 9:1335–1340

    Article  PubMed  Google Scholar 

  • van der Wielen PW, Bolhuis H, Borin S, Daffonchio D, Corselli C, Giuliano L, D’Auria G, de Lange GJ, Huebner A, Varnavas SP, Thomson J, Tamburini C, Marty D, McGenity TJ, Timmis KN (2005) The enigma of prokaryotic life in deep hypersaline anoxic basins. Science 307:121–123

    Article  PubMed  Google Scholar 

  • van Hoek AH, van Alen TA, Sprakel VS, Leunissen JA, Brigge T, Vogels GD, Hackstein JH (2000) Multiple acquisition of methanogenic archaeal symbionts by anaerobic ciliates. Mol Biol Evol 17:251–258

    Article  PubMed  Google Scholar 

  • Yakimov MM, Giuliano L, Cappello S, Denaro R, Golyshin PN (2007a) Microbial community of a hydrothermal mud vent underneath the deep-sea anoxic brine lake Urania (eastern Mediterranean). Orig Life Evol Biosph 37:177–188

    Article  PubMed  Google Scholar 

  • Yakimov MM, La Cono V, Denaro R, D’Auria G, Decembrini F, Timmis KN, Golyshin PN, Giuliano L (2007b) Primary producing prokaryotic communities of brine, interface and seawater above the halocline of deep anoxic lake L’Atalante, eastern Mediterranean Sea. ISME J 1:743–755

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work is part of a collaboration with the Stoeck laboratory at University of Kaiserslautern, Germany; the Kormas laboratory at University of Thessaly, Greece; and the Yakimov laboratory at Istituto per l’Ambiente Marino Costiero, CNR, Messina, Italy. We would like to thank the captains and crews of the R/V Oceanus, R/V Atlantis, and R/V Urania for their hard work to assure the success of our sampling objectives. VE would like to acknowledge funding by NSF OCE-0849578.

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Correspondence to Virginia P. Edgcomb .

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Edgcomb, V.P., Orsi, W.D. (2013). Microbial Eukaryotes in Hypersaline Anoxic Deep-Sea Basins. In: Seckbach, J., Oren, A., Stan-Lotter, H. (eds) Polyextremophiles. Cellular Origin, Life in Extreme Habitats and Astrobiology, vol 27. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6488-0_23

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