Abstract
Salinity is an important factor when exploring the limits known for life. Therefore, hypersaline systems have attracted much attention in recent years. In this study, we investigated the protistan diversity and community composition in two natural salt evaporation ponds (27–30% salinity) located in an ancient volcanic crater on the Cape Verde island Sal using high-throughput DNA sequencing. Our study revealed a broad range of protistan taxa and a high taxonomic diversity within the Ciliophora, Dinophyceae, and Chlorophyta. We detected a total of 23 Dinophyceae families, although Dinophyceae were generally considered to be only this diverse in aquatic environments of less than 10% salinity. Moreover, we uncovered a high degree of genetic novelty in this habitat. The mean similarity of all detected OTUs to previously described sequences was only 93.6%. These findings strongly dispute the traditional view that extreme hypersaline environments generally maintain low protistan diversity. A meta-analysis covering our and previously published data from other inland and coastal salt ponds clearly showed that our samples clustered according to salinity and not biogeography. This result further supports the claim that salinity is a major transition boundary for protistan communities, regardless of their biogeographic origin.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1006/jmbi.1990.9999
Boomer I, Aladin N, Plotnikov I, Whatley R (2000) The palaeolimnology of the Aral Sea: a review. Quaternary Sci Rev 19:1259–1278. https://doi.org/10.1016/S0277-3791(00)00002-0
Buck K, Barry J, Simpson A (2000) Monterey Bay cold seep biota: euglenozoa with chemoautotrophic bacterial epibionts. Eur J Protistol 36:117–126
Butschinsky P (1897) Die Protozoenfauna der Salzseelimane bei Odessa. Zool Anz 20:194–197
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
Casamayor EO, Triadó-Margarit X, Castaneda C (2013) Microbial biodiversity in saline shallow lakes of the Monegros Desert, Spain. FEMS Microb Ecol 85:503–518. https://doi.org/10.1111/1574-6941.12139
Clark DR, Mathieu M, Mourot L, Dufossé L, Underwood GJC, Dumbrell AJ, McGenity TJ (2017) Biogeography at the limits of life: do extremophilic microbial communities show biogeographical regionalization? Glob Ecol Biogeogr 26:1435–1446. https://doi.org/10.1111/geb.12670
Curry R, Dickson B, Yashayaev I (2003) A change in the freshwater balance of the Atlantic Ocean over the past four decades. Nature 426:826. https://doi.org/10.1038/nature02206
de Vargas C, Audic S, Henry N, Decelle J, Mahe F, Logares R, Lara E, Berney C, Le Bescot N, Probert I, Carmichael M, Poulain J, Romac S, Colin S, Aury JM, Bittner L, Chaffron S, Dunthorn M, Engelen S, Flegontova O, Guidi L, Horak A, Jaillon O, Lima-Mendez G, Lukes J, Malviya S, Morard R, Mulot M, Scalco E, Siano R, Vincent F, Zingone A, Dimier C, Picheral M, Searson S, Kandels-Lewis S, Acinas SG, Bork P, Bowler C, Gorsky G, Grimsley N, Hingamp P, Iudicone D, Not F, Ogata H, Pesant S, Raes J, Sieracki ME, Speich S, Stemmann L, Sunagawa S, Weissenbach J, Wincker P, Karsenti E, Tara Oceans C (2015) Eukaryotic plankton diversity in the sunlit ocean. Science 348:6237. https://doi.org/10.1126/science.1261605
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27:2194–2200. https://doi.org/10.1093/bioinformatics/btr381
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. https://doi.org/10.1007/s00792-008-0206-2
Elloumi J, Carrias JF, 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. https://doi.org/10.1016/j.ecss.2005.10.011
Elloumi J, Carrias JF, Ayadi H, Sime-Ngando T, Bouain A (2009) Communities structure of the planktonic halophiles in the solar saltern of Sfax, Tunisia. Estuar Coast Shelf Sci 81:19–26. https://doi.org/10.1016/j.ecss.2008.09.019
Entz G (1879) Ueber einige Infusorien des Salzteiches zu Szamosfalva. Természetr Füz 3:33–72
Entz G (1904) Die Fauna der kontinentalen Kochsalzwässer. Math Naturwissen Ber Ungarn 19:89–124
Filker S, Gimmler A, Dunthorn M, Mahé F, Stoeck T (2015) Deep sequencing uncovers protistan plankton diversity in the Portuguese Ria Formosa solar saltern ponds. Extremophiles 19:283–295. https://doi.org/10.1007/s00792-014-0713-2
Filker S, Forster D, Weinisch L, Mora-Ruiz M, Gonzalez B, Farias ME, Rossello-Mora R, Stoeck T (2017) Transition boundaries for protistan species turnover in hypersaline waters of different biogeographic regions. Environ Microbiol 19:3186–3200. https://doi.org/10.1111/1462-2920.13805
Florentin MR (1899) Études sur la fauna des mares salées de Lorraine. Ann Sci Nat Zool 10:209–350
Foissner W, Jung JH, Filker S, Rudolph J, Stoeck T (2014a) Morphology, ontogenesis and molecular phylogeny of Platynematum salinarum nov spec., a new scuticociliate (Ciliophora, Scuticociliatia) from a solar saltern. Eur J Protistol 50:174–184. https://doi.org/10.1016/j.ejop.2013.10.001
Foissner W, Filker S, Stoeck T (2014b) Schmidingerothrix salinarum nov. spec. is the molecular sister of the large oxytrichid clade (Ciliophora, Hypotricha). J Eukaryot Microbiol 61:61–74. https://doi.org/10.1111/jeu.12087
Fotedar R, Stoeck T, Filker S, Fell JW, Agatha S, Al Marri M, Jiang J (2016) Description of the halophile Euplotes qatarensis nov. spec. (Ciliophora, Spirotrichea, Euplotida) isolated from the hypersaline Khor Al-Adaid Lagoon in Qatar. J Eukaryot Microbiol 63:578–590. https://doi.org/10.1111/jeu.12305
Fuhrman JA (2009) Microbial community structure and its functional implications. Nature 459:193–199. https://doi.org/10.1038/nature08058
Ghai R, Pasic L, Fernández AB, Martin-Cuadrado AB, McMahon KD, Papke RT, Stepanauskas R, Rodriguez-Brito B, Rohwer F, Sánchez-Porro C, Ventosa A, Rodríguez-Valera F (2011) New abundant microbial groups in aquatic hypersaline environments. Sci Rep 1:135. https://doi.org/10.1038/srep00135
Gong J, Dong J, Liu X, Massana R (2013) Extremely high copy numbers and polymorphisms of the rDNA operon estimated from single cell analysis of Oligotrich and Peritrich Ciliates. Protist 164:369–379. https://doi.org/10.1016/j.protis.2012.11.006
Gunde-Cimerman N, Oren A, Plemenitaš A (2005) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya, vol 9. Springer, Dordrecht
Harding T, Simpson AGB (2018) Recent advances in halophilic protists. J Eukaryot Microbiol. https://doi.org/10.1111/jeu.12495
Harris JK, Caporaso JG, Walker JJ, Spear JR, Gold NJ, Robertson CE, Hugenholtz P, Goodrich J, McDonald D, Knights D, Marshall P, Tufo H, Knight R, Pace NR (2012) Phylogenetic stratigraphy in the Guerrero Negro hypersaline microbial mat. ISME J 1:11. https://doi.org/10.1038/ismej.2012.79
Heidelberg KB, Nelson WC, Holm JB, Eisenkol N, Andrade K, Emerson JB (2013) Characterization of eukaryotic microbial diversity in hypersaline Lake Tyrrell, Australia. Front Microbiol 4:115. https://doi.org/10.3389/fmicb.2013.00115
Javor B (1989) Hypersaline environments. Microbiology and biogeochemistry. Springer, Berlin
Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439. https://doi.org/10.1890/06-1736.1
Kirby H (1932) Two protozoa from brine. Trans Am Microsc Soc 51:8–15
Kunte HJ, Trüper H, Stan-Lotter H (2002) Halophilic microorganisms. In: Horneck G, Baumstark-Khan C (eds) Astrobiology: the quest for the conditions of life. Springer, Berlin, pp 185–200
Layburn-Parry J, Bell EM, Roberts EC (2000) Protozoan growth rates in Antarctic lakes. Polar Biol 23:445–451
Lei Y, Xu K, Choi JK, Hong HP, Wickham SA (2009) Community structure and seasonal dynamics of planktonic ciliates along salinity gradients. Eur J Protistol 45:305–319. https://doi.org/10.1016/j.ejop.2009.05.002
Logares R, Audic S, Bass D, Bittner L, Boutte C, Christen R, Claverie JM, Decelle J, Dolan JR, Dunthorn M, Edvardsen B, Gobet A, Kooistra WHCF, Mahe F, Not F, Ogata H, Pawlowski J, Pernice MC, Romac S, Shalchian-Tabrizi K, Simon N, Stoeck T, Santini S, Siano R, Wincker P, Zingone A, Richards TA, de Vargas C, Massana R (2014) Patterns of rare and abundant marine microbial eukaryotes. Curr Biol 24:813–821. https://doi.org/10.1016/j.cub.2014.02.050
Mahé F, Rognes T, Quince C, de Vargas C, Dunthorn M (2015) Swarm v2: highly-scalable and high-resolution amplicon clustering. Peer J. https://doi.org/10.7717/peerj.1420
Massana R, Gobet A, Audic S, Bass D, Bittner L, Boutte C, Chambouvet A, Christen R, Claverie JM, Decelle J, Dolan JR, Dunthorn M, Edvardsen B, Forn I, Forster D, Guillou L, Jaillon O, Kooistra WHCF, Logares R, Mahe F, Not F, Ogata H, Pawlowski J, Pernice MC, Probert I, Romac S, Richards T, Santini S, Shalchian-Tabrizi K, Siano R, Simon N, Stoeck T, Vaulot D, Zingone A, de Vargas C (2015) Marine protist diversity in European coastal waters and sediments as revealed by high-throughput sequencing. Environ Microbiol 17:4035–4049. https://doi.org/10.1111/1462-2920.12955
Namyslowski B (1913) Über unbekannte halophile Mikroorganismen aus dem Innern des Salzbergwerkes Wieliczka. Bull Int Acad Sci Krakow B 3(4):88–104
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2017) vegan: Community Ecology Package. R package version 2.4–4. http://CRAN.R-project.org/package=vegan. Accessed Oct 2017
Oren A (2002) Diversity of halophilic microorganisms: environments, phylogeny, physiology, and applications. J Ind Microbiol Biot 28:56–63. https://doi.org/10.1038/sj.jim.7000176
Oren A (2008) Microbial life at high salt concentrations: phylogenetic and metabolic diversity. Saline Syst 4:2. https://doi.org/10.1186/1746-1448-4-2
Pan H, Stoeck T (2017) Redescription of the halophile ciliate, Blepharisma halophilum Ruinen, 1938 (Ciliophora, Heterotrichea, Heterotrichida) shows that the genus Blepharisma is non-monophyletic. Eur J Protistol 61:20–28. https://doi.org/10.1016/j.ejop.2017.07.004
Park JS, Cho BC, Simpson AGB (2006) Halocafeteria seosinensis gen. et sp nov (Bicosoecida), a halophilic bacterivorous nanoflagellate isolated from a solar saltern. Extremophiles 10:493–504. https://doi.org/10.1007/s00792-006-0001-x
Patterson DJ, Simpson AGB (1996) Heterotrophic flagellates from coastal marine and hypersaline sediments in Western Australia. Eur J Protistol 32:423–448. https://doi.org/10.1016/S0932-4739(96)80003-4
Pedrós-Alió C (2004) Trophic ecology of solar salterns. In: Ventosa A (ed) Halophilic microorganisms. Spriner-Verlag, Berlin, pp 33–48
Pedrós-Alió C (2005) Diversity of microbial communities: the case of solar salterns. In: Gunde-Cimerman N, Oren A, Plemenitaš A (eds) Adaptation to life at high salt concentrations in Archaea, Bacteria, and Eukarya. Springer, Netherlands, pp 71–90
Pedrós-Alió C (2012) The rare bacterial biosphere. Annu Rev Mar Sci 4:449–466. https://doi.org/10.1146/annurev-marine-120710-100948
Pedrós-Alió C, Calderon-Paz JI, MacLean MH, Medina G, Marrase C, Gasol JM, Guixa-Boixereu N (2000) The microbial food web along salinity gradients. FEMS Microbiol Ecol 32:143–155. https://doi.org/10.1111/j.1574-6941.2000.tb00708.x
Por F (1980) A classification of hypersaline waters, based on trophic criteria. Mar Ecol 1:121–131
Ruinen J (1938) Notizen über Salzflagellaten. II. Über die Verbreitung der Salzflagellaten. Arch Protistenkd 90:210–258
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. https://doi.org/10.1101/gr.1239303
Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Anton Leeuw Int J G 81:293–308
Sime-Ngando T, Grolière CA (1991) Quantitative effects of fixatives on the storage of freshwater planktonic ciliates. Arch Protistenk 140:109–120
Sime-Ngando T, Hartmann HJ, Grolière CA (1990) Rapid quantification of planktonic ciliates: comparison of improved live counting with other methods. Appl Environ Microbiol 56:2234–2242
Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR, Arrieta JM, Herndl GJ (2006) Microbial diversity in the deep sea and the underexplored “rare biosphere”. Proc Natl Acad Sci USA 103:12115–12120. https://doi.org/10.1073/pnas.0605127103
Stock A, Breiner HW, Pachiadaki M, Edgcomb V, Filker S, La Cono V, Yakimov MM, Stoeck T (2012) Microbial eukaryote life in the new hypersaline deep-sea basin Thetis. Extremophiles 16:21–34. https://doi.org/10.1007/s00792-011-0401-4
Stoeck T, Bass D, Nebel M, Christen R, Jones MDM, Breiner HW, Richards TA (2010) Multiple marker parallel tag environmental DNA sequencing reveals a highly complex eukaryotic community in marine anoxic water. Mol Ecol 19:21–31. https://doi.org/10.1111/j.1365-294X.2009.04480.x
Triadó-Margarit X, Casamayor EO (2013) High genetic diversity and novelty in planktonic protists inhabiting inland and coastal high salinity water bodies. FEMS Microbiol Ecol 85:27–36. https://doi.org/10.1111/1574-6941.12095
Ventosa A (2006) Unusual micro-organisms from unusual environments. In: Logan NA, Lappin-Scott HM, Oyston P (eds) SGM Symposium 66: Prokaryotic diversity—mechanisms and significance. Cambridge University Press, Cambridge, pp 223–253
Volcani B (1944) The microorganisms of the Dead Sea. Papers collected to commemorate the 70th anniversary of Dr. Chaim Weizmann. Daniel Sieff Research Institute, Rehovoth, pp 71–85
Wang J, Wang F, Chu L, Wang H, Zhong Z, Liu Z, Gao J, Duan H (2014) High genetic diversity and novelty in eukaryotic plankton assemblages inhabiting saline lakes in the Qaidam basin. PLoS One 9:e112812. https://doi.org/10.1371/journal.pone.0112812
Weber APM, Horst RJ, Barbier GG, Oesterhelt C (2007) Metabolism and metabolomics of eukaryotes living under extreme conditions. Int Rev Cytol 256:1–34. https://doi.org/10.1016/s0074-7696(07)56001-8
Wu Q, Chatzinotas A, Wang J, Boenigk J (2009) Genetic diversity of eukaryotic plankton assemblages in Eastern Tibetan Lakes differing by their salinity and altitude. Microb Ecol 58:569–581. https://doi.org/10.1007/s00248-009-9526-8
Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate illumina Paired-End reAd mergeR. Bioinformatics 30:614–620. https://doi.org/10.1093/bioinformatics/btt593
Zhao F, Xu K (2017) Distribution of ciliates in intertidal sediments across geographic distances: a molecular view. Protist 168:171–182. https://doi.org/10.1016/j.protis.2017.01.001
Zhao F, Filker S, Xu K, Huang P, Zheng S (2017) Patterns and drivers of vertical distribution of the ciliate community from the surface to the abyssopelagic zone in the Western Pacific Ocean. Front Microbiol 8:2559. https://doi.org/10.3389/fmicb.2017.02559
Acknowledgements
This research was funded by a grant from the TU Nachwuchsring to SF. Research of FZ was supported by the China Scholarship Council (CSC, No. 201604910395). Samples were collected during a research cruise with R/V Meteor (M118) funded by the DFG Senatskommission. We thank Thorsten Stoeck (University of Technology Kaiserslautern) for his help with sample collection. Data analysis was performed on the high-performance computing cluster “Elwetritsch” at the University of Kaiserslautern supported by an AHRP Grant to SF.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by A. Oren.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhao, F., Filker, S. Characterization of protistan plankton diversity in ancient salt evaporation ponds located in a volcanic crater on the island Sal, Cape Verde. Extremophiles 22, 943–954 (2018). https://doi.org/10.1007/s00792-018-1050-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00792-018-1050-7