Population dynamics of amoeboid protists in a tropical desert: seasonal changes and effects of vegetation and soil conditions

Horacio Pérez-Juárez,

Angélica Serrano-Vázquez,

Enrique Lara,

Cecilia Ximénez,

Héctor Godínez-Alvarez,

Salvador Rodríguez-Zaragoza,

Luis E. Eguiarte,

Mayra M. Hernández Moreno,

Leonardo D. Fernández,

Liliana Rojas-Velázquez,

Patricia Morán,

Mariela Castillo,

Víctor M. Rivera Aguilar


In arid environments, protist diversity is higher in soil covered by vegetation than in bare soil and is also likely to vary in line with the marked seasonal patterns; however, these patterns have not been explored in detail in arid zones. Herein, we used culture – and morphological-based approaches to describe patterns of amoeboid protist diversity in  vegetated and bare soil areas from the intertropical desert of Tehuacán, Mexico, during dry and wet seasons. Overall, 27 protist species belonging to Amoebozoa, Discoba and Rhizaria were retrieved using culture-dependent methods. Among the soil protist groups found, Discoba (principally represented by Heterolobosea) was always the most prevalent taxa. Protist diversity was different between soil with vegetation and bare soil, principally during the dry season. Moreover, the electrical conductivity and pH of the soil were correlated with the protist species during the wet season. Our results support the hypothesis that soil protist diversity patterns exhibit a seasonal variation between dry  and wet seasons. This seasonal variation likely relies on water availability, although the role of other environmental factors cannot be completely ruled out. In addition, the soils with vegetation could be a refuge for the amoeboid protists during the harsh soil conditions of dry seasons.

Słowa kluczowe: Heterolobosea, seasonal variation, soil microhabitat, soil protist, Tehuacán desert.

Adl, S. M., Simpson, A. G., Lane, C.E., Lukeš, J., Bass, D., Bowser, S. S., Brown M. W., Burki F., Dunthorn M., Hampl V., Heiss A., Hoppenrath M., Lara E., Le Gal L., Lynn D. H., McManus H., Mitchell A. D. E., Mozley-Stanridge S. E., Parfrey L. W., Pawlowski J., Rueckert S., Shadwick L., Schoch C. L., Smirnov A., Spiegel F. W. (2012). The revised classification of eukaryotes. J Eukaryot. Microbiol59: 429-514

Adl, S. M., Bass, D., Lane, C. E., Lukeš, J., Schoch C. L., Smirnov A., Agatha, S., Berney, C., Brown M. W., Burki F., Cardenas, P., Cepicka, I., Chistyakova, L., del Campo, J., Dunthorn M., Edvarsen, B., Eglit, Y., Guillou, L., Hampl, V., Heisss, A. A., Hoppenrath, M., James, T. Y., Karpov, S., Kim, E., Kolisko, M., Kudryavtsev, A., Lahr, D.J.G., Lara, E., Le Gall, L., Lynn D. H., Mann, D. G., Massana, R., Mitchell A. D. E., Morrow, C., Soo, J., Pawlowski J., Powell, M. J., Richter, D. J., Rueckert, S., Shadwick, L., Shimano, S., Spiegel F. W., Torruella, G., Youssef, N., Zlatogursky, V., Zhang, Q. (2018). Revisions to the classification, nomenclature, and diversity of eukaryotes. J Eukaryot. Microbiolhttps://doi.org/10.1111/jeu.12691

Anderson O. R. (2000) Abundance of terrestrial gymnamoebae at a northeastern U. S. site: A four-year study, including the El Nino winter of 1997–1998. J. Eukaryot. Microbiol

47: 148-155

Anderson O. R., Wang W. E. N., Faucher S. P., Bi K., Shuman H. A. (2011) A new

heterolobosean amoeba Solumitrus palustris n. g., n. sp. isolated from freshwater

marsh soil. J. Eukaryot. Microbiol. 58: 60-67

Austin A.T., Yahdjian L., Stark J.M., Belnap J., Porporato A., Norton U., Ravetta D.A., Schaeffer S.M. (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141: 221–235

Avis T.J., Gravel V., Antoun H., Tweddell R. (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol. Biochem.40: 1733-1740

Bamforth, S. S. (1963) Limnetic protozoa of southeastern Louisiana.  Proc. Louisiana Acad. Sci. 26: 120-134

Bamforth S. S. (2008) Protozoa of biological soil crusts of a cool desert in Utah. J. Arid Environ. 72: 722–729

Barness G., Rodríguez S., Shmueli I., Steinberger Y. (2009) Vertical distribution of a soil microbial community as affectd by plant ecophysiological adaptation in a desert system. Microbiol. Ecol. 57: 36-49

Bass P., Bischoff P. J. (2001) Seasonal variability in abundance and diversity of soil Gymnamoebae along a short transect in Southeastern USA. J. Eukaryot. Microbiol. 48: 475–479

Bates, R. G. (1954) Electrometric pH Determinations. John Wiley & Sons, Inc.

Bouyoucos G. J. (1962) Hydrometer method improved for making particle size analyses of soils. Agron. J54: 464–465

Bonkowski M. (2004) Protozoa and plant growth: the microbial loop in soil revisited. New Phytologist. 162: 617–631

Braschi I., Ciavatta C., Giovannini C., Gessa C. (2003) Combined effect of water and organic matter on phosphorus availability in calcareous soils. Nut Cycl Agroecosys67: 67-74

Brown S., De Jonckheere J. F. (1999) A reevaluation of the amoeba genus Vahlkampfia based on SSUrDNA sequences. Eur. J. Protistol. 35: 49–54

Cajuste L. J. (1986) El fósforo aprovechable en los suelos. Cuadernos de Edafología. Vol. 6 Centro de Edafología, Colegio de Postgraduados, México.

Colwell R. K. (2013) EstimateS: Statistical estimation of richness and shared species from samples. Version 9.

Dávila, P., Arizmendi, M. D. C., Valiente-Banuet, A., Villaseñor, J. L., Casas, A., Lira, R. (2002) Biological diversity in the Tehuacán-Cuicatlán Valley, Mexico. Biod.con11: 421-442

De Jonckheere J. F., Baumgartner M., Eberhardt S., Opperdoes F. R., Stetter K. O. (2011a) Oramoeba fumarolia gen. nov., sp nov., a new marine heterolobosean amoeboflagellate growing at 54 degrees C. Eur. J. Protistol. 47: 16–23

De Jonckheere J. F., Murase J., Opperdoes F. R. (2011b) A new thermophilic heterolobosean amoeba, Fumarolamoeba ceborucoi, gen. nov., sp nov., isolated near a fumarole at a volcano in Mexico. Acta Protozool. 50: 41–48

Dobson P. J., Robinson B. S., Rowan-Kelly, B. (1997) New thermophilic Naegleria species (Heterolobosea: Vahlkampfiidae) from Australia and Asia: Allozyme, morphometric and physiological characterisation. Acta Protozool. 36: 261–271

Dumack K., Koller R., Weber B., Bonkowski M. (2016) Estimated abundance and diversity of heterotrophic protists in South African biocrusts. S Afr J Sci. 112: 56-60

Ekelund F., Ronn R., (1994) Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol. Rev. 15: 321–353

Fahrni J. F., Bolivar I., Berney C., Nassonova E., Smirnov A., Pawlowski J. (2003) Phylogeny of lobose amoebae based on actin and small-subunit ribosomal RNA genes. Mol. Biol. Evol20: 1881–1886

Fernández L. D. (2015) Source–sink dynamics shapes the spatial distribution of soil protists in an arid shrubland of northern Chile. J. Arid Environ. 113: 121–125

Foissner W. (2011) Dispersal of protist: the role of cyst and human introduction. In Biogeography of Microscopic Organisms: is Everything Small Everywhere? Fontaneto, D., ed. Systematics Association and Cambridge University Press, Cambridge, UK. pp 61–87

Foster R. C., Dormaar J. F. (1991) Bacteria-grazing amoebae in situ in the rhizosphere. Biol. Fertil. Soils11: 83–87

Geisen S., Fiore-Donno A. M., Walochnik J., Bonkowski M. (2014) Acanthamoeba everywhere: high diversity of Acanthamoeba in soils. Parasitol. Res. 113: 3151–3158

Geisen S., Bonkowski M., Zhang J., De Jonckheere J. F. (2015). Heterogeneity in the genus Allovahlkampfia and the description of the new genus Parafumarolamoeba (Vahlkampfiidae; Heterolobosea). Eur j protisto, 51:335-349

Geisen S., Koller R., Hunninghaus M., Dumack K., Urich T., Bonkowski M. (2016) The soil food web revisited: Diverse and widespread mycophagous soil protists. Soil Biol. Biochem. 94: 10–18

Geisen S., Mitchell E. A. D., Wilkinson D. M., Adl S., Bonkowski M., Brown M. W., Fiore-Donno A. M., Heger T. J., Jassey V. E. J., Krashevska V., Lahr D. J. G., Marcisz K., Mulot M., Payne R., Singer D., Anderson O. R., Charman D. J., Ekelund F., Griffiths B. S., Rønn R., Smirnov A., Bass D., Belbahri L., Berney C., Blandenier Q., Chatzinotas A., Clarholm M., Dunthorn M., Feest A., Fernández L. D., Foissner W., Fournier B., Gentekaki E., Hájek M., Helder J., Jousset A., Koller R., Kumar S., La Terza A., Lamentowicz M., Mazei Y., Santos S. S., Seppey C. V. W., Spiegel F. W., Walochnik J., Winding A., Lara E. (2017) Soil protistology rebooted: 30 fundamental questions to start with. Soil Biol. Biochem. 111: 94–103

Geisen S., Mitchell E. A., Adl S., Bonkowski M., Dunthorn M., Ekelund F., Fernández L. D., Jousset A., Krashevska V., Singer D., Spiegel F. W., Walochnik J., Lara E. (2018) Soil protists: a fertile frontier in soil biology research. FEMS Microbiol rev. doi:10.1093/femsre/fuy006

Griffiths B.S., Bonkowski M., Roy J., Ritz K. (2001) Functional stability, substrateutilisation and biological indicators of soils following environmental impacts. Appl. Soil Ecol. 16: 49–61

Lanzén A., Epelde L., Blanco F., Martín I., Artetxe U., Garbisu C. (2016) Multi-targeted metagenetic analysis of the influence of climate and environmental parameters on soil microbial communities along an elevational gradient. Sci rep6: 28257

Li C.,  Li Y., Ma J. (2011) Spatial heterogeneity of soil chemical properties at fine scale induced by Haloxylon ammodendron (Chenopodiaceae) plants in a sandy desert. Ecol. Res. 26: 385-394

Li, J., Lin, J., Pei, C., Lai, K., Jeffries, T. C., Tang, G. (2018).Variation of soil bacterial communities along a chronosequence of Eucalyptus plantation. PeerJ6, e5648

López-Galindo F., Muñoz-Iniestra D., Hernández-Moreno M., Soler-Aburto A., Castillo-López M. D. C., Hernandez-Arzate I. (2003) Análisis integral de la toposecuencia y su influencia en la distribución de la vegetación y la degradación del suelo en la subcuenca de Zapotitlán Salinas, Puebla. B. Soc. Geol. Mex. 56: 19–41

Mayzlish-Gati E., Steinberger Y. (2007) Ameba community dynamics and diversity in a desert ecosystem. Biol. Fertil. Soils. 43: 357–366

Medina H., García J., Núñez D. (2007) El método del hidrómetro: base teórica para su empleo en la determinación de la distribución del tamaño de partículas de suelo. Revista Ciencias Técnicas Agropecuarias 16: 19–24

Oksanen J., Blanchet F. G., Kindt R., Legendre P., Minchin P. R., O’hara R. B., Oksanen M. J. (2013) Package ‘vegan’. Communityecology package, version, 2.9.

Olsen R. S., Cole V. C., Wantanabe F. S., Dean L. A. (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. United State Department of Agriculture, Washington, DC.

Ortiz V. B., Ortiz A. (1980) Edafologia, 3rd ed. Universidad Autónoma Chapingo, México.

Osorio-Beristain O., Valiente-Banuet A., Dávila P., Medina R. (1996) Types of vegetation and βdiversity at the Valle de Zapotitlán de las Salinas, Puebla, Mexico. Bot.  Sci. 59: 35–58

Page F. C. (1976) Illustrated key to freshwater and soil amoebae. Freshwater Biol. Ass. Ambleside.

Page F. C. (1988) A new key to freshwater and soil gymnamoebae: with instructions for culture. Freshwater Biol. Ass. Ambleside.

Pawlowski J., Burki F. (2009) Untangling the phylogeny of amoeboid protists. J. Eukaryot. Microbiol. 56: 16–25

Pérez-Juárez H., Serrano-Vázquez A., Kosakyan A., Mitchell E. A., Aguilar V. M. R., Lahr D. J. G., Hernández M. M. M., Macías C. H., Eguiarte L. E., Lara E. (2017) Quadrulella texcalense sp. nov. from a Mexican desert: an unexpected new environment for hyalospheniid testate amoebae. Eur. J. Protistol. 61:253-264

Pugnaire F. I., ArmasC., Valladares F. (2004) Soil as a mediator in plant-plant interaction in a semi-arid community. J. Veg. Sci. 15:85-92

Robinson B. S., Bamforth S. S., Dobson P. J. (2002) Density and diversity of protozoa in some arid Australian soils. J. Eukaryot. Microbiol. 49: 449–453

Rodríguez-Zaragoza S., Steinberger Y. (2004) Seasonal dynamics of amoebae in the root canopy of Zygophyllum dumosum in the Negev Desert, Israel. Pedobiologia 48: 277–281

Rodríguez-Zaragoza S., Mayzlish E., Steinberger Y. (2005a). Vertical distribution of the free-living amoeba population in soil under desert shrubs in the Negev desert, Israel. Appl. Environ. Microbiol. 71: 2053–2060

Rodríguez-Zaragoza S., Mayzlish E., Steinberger Y. (2005b) Seasonal changes in free-living amoeba species in the root canopy of Zygophyllum dumosum in the Negev Desert, Israel. Microb. Ecol49: 134–141

Shen C., Liang W., Shi Y., Lin X., Zhang H., Wu X., Xie G., Chain P., Grogan P., Chu H. (2014) Contrasting elevational diversity patterns between eukaryotic soil microbes and plants. Ecology 95:3190–3202

Seppey C. V., Singer D., Dumack K., Fournier B., Belbahri L., Mitchell E. A., Lara E. (2017) Distribution patterns of soil microbial eukaryotes suggests widespread algivory by phagotrophic protists as an alternative pathway for nutrient cycling. Soil Biol. Biochem112:68–76

Serrano-Vázquez A., Rodríguez-Zaragoza, S., Pérez-Juárez, H., Bazán-Cuenca, J., Rivera-Aguilar, V. M., Durán, A. 2013. Physical and chemical variations of the soil under two desert shrubs in Tehuacan, Mexico. Soil Sci. 178. 87–103

Smirnov, A. V., Brown, S. (2004) Guide to the methods of study and identification of soil Gymnamoebae. Protistology3: 148–190

Stewart, J. W. B., Tiessen, H. (1987) Dynamics of soil organic phosphorus.

Biogeochemistry4: 41–60

Sylvain, Z. A., Wall, D. H. (2011) Linking soil biodiversity and vegetation: Implications for a changing planet. Am. J. Bot.98: 517–527

Tunesi S., Poggi V., Gessa C. (1999) Phosphate adsorption and precipitation in calcareous soils: The role of calcium ions in solution and carbonate minerals. Nutr. Cycl. Agroecosyst. 53: 219–227

Valiente-Banuet, A., Casas, A., Alcántara, A., Dávila, P., Flores-Hernández, N., del Coro Arizmendi, M., Ramírez, J.O., (2000) The vegetation of the Valley of Tehuacan-Cuicatlan. Bot. Sci.67: 25–74

Villaseñor, J. L., Davila, P., Chiang, F. (1990) Fitogeografía del valle de Tehuacán-Cuicatlán. (Phytogeography of the Tehuacan-Cuicatlan valley). Bol. Soc. Bot. Mex.50 135–149

Walkley , A., Black, I. A. (1934) An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil sci. 37:29-–8

Whitford, W. G. (2002) Ecology of desert systems. Academic Press, London, UK.

Willard, H. H., Merritt, L. L., Dean, J. A. (1958). Instrumental Methods of Analysis, 3rd ed. Van Nostrand, Princeton, USA.

Czasopismo w darmowym dostępie.

Czasopismo ukazuje się w sposób ciągły on-line.
Pierwotną formą czasopisma jest wersja elektroniczna.