Metacommunity analysis of amoeboid protists in grassland soils

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Fiore Donno, Anna Maria ^a   Weinert, Jan ^a   Wubet, Tesfaye ^b,c   Bonkowski, Michael ^a  

^a UNIVERSITY OF COLOGNE   (Germany)

^b HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

^c GERMAN CENTRE FOR INTEGRATIVE BIODIVERSITY RESEARCH IDIV HALLE JENA LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACANTHAMOEBA; AMOEBA (LIFE CYCLE STAGE); BIODIVERSITY; FILTRATION; GENETIC VARIABILITY; GENUS; GERMANY; GRASSLAND; MAJOR CLINICAL STUDY; MYXOGASTRIA; PROTIST; RNA GENE; SAMPLING; SOIL; CLUSTER ANALYSIS; GENETIC VARIATION; GENETICS; METAGENOMICS; PARASITOLOGY; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS;

SOIL;

AMOEBA; CLUSTER ANALYSIS; GENETIC VARIATION; GRASSLAND; METAGENOMICS; PHYLOGENY; PRINCIPAL COMPONENT ANALYSIS; SOIL;

EID: 84954065636     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep19068     Document Type: Article

References (80)

1. Bonkowski, M., Griffiths, B. S. & Scrimgeour, C. Substrate heterogeneity and microfauna in soil organic 'hotspots' as determinants of nitrogen capture and growth of ryegrass. Appl. Soil Ecol. 14, 37-53 (2000).
2. Rønn, R., McCaig, A. E., Griffiths, B. S. & Prosser, J. I. Impact of protozoan grazing on bacterial community structure in soil microcosms. Appl. Environ. Microbiol. 68, 6094-6105 (2002).
3. Murase, J. & Frenzel, P. Selective grazing of methanotrophs by protozoa in a rice field soil. FEMS Microbiol. Ecol. 62, 408-414 (2008).
4. Saleem, M., Fetzer, I., Dormann, C. F., Harms, H. & Chatzinotas, A. Predator richness increases the effect of prey diversity on prey yield. Nat. Commun. 3, 1305 (2012).
5. Ekelund, F. & Rønn, R. Notes on protozoa in agricultural soil with emphasis on heterotrophic flagellates and naked amoebae and their ecology. FEMS Microbiol. Rev. 15, 321-353 (1994).
6. Foissner, W. Soil protozoa as bioindicators: pros and cons, methods, diversity, representative examples. Agric. Ecosyst. Environ. 74, 95-112 (1999).
7. Fredslund, L., Ekelund, F., Jacobsen, C. S. & Johnsen, K. Development and application of a most-probable-number-PCR assay to quantify flagellate populations in soil samples. Appl. Environ. Microbiol. 67, 1613-1618 (2001).
8. Pawlowski, J. The new micro-kingdoms of eukaryotes. BMC Biol. 11, 40 (2013).
9. Elliott, E. & Coleman, D. C. Soil protozoan dynamics in a shortgrass prairie. Soil Biol. Biochem. 9, 113-118 (1977).
10. Clarholm, M. Protozoan grazing of bacteria in soil - impact and importance. Microb. Ecol. 7, 343-350 (1981).
11. O'Brien, H. E., Parrent, J. L., Jackson, J. A., Moncalvo, J.-M. & Vilgalys, R. Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71, 5544-5550 (2005).
12. Fierer, N. et al. Metagenomic and small-subunit rRNA analyses reveal the genetic diversity of bacteria, Archaea, fungi, and viruses in soil. Appl. Environ. Microbiol. 73, 7059-7066 (2007).
13. Buée, M. et al. 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. New Phytol. 184, 449-456 (2009).
14. Gottel, N. R. et al. Distinct microbial communities within the endosphere and rhizosphere of Populus deltoides roots across contrasting soil types. Appl. Environ. Microbiol. 77, 5934-5944 (2011).
15. Pawlowski, J. et al. CBOL Protist Working Group: Barcoding eukaryotic richness beyond the animal, plant and fungal kingdoms. PLoS Biology 10, e1001419 (2012).
16. Jeon, S. et al. Environmental rRNA inventories miss over half of protistan diversity. BMC Microbiol. 8, 222-235 (2008).
17. Lentendu, G. et al. Effects of long-term differential fertilization on eukaryotic microbial communities in an arable soil: a multiple barcoding approach. Mol. Ecol. 23, 3341-3355 (2014).
18. Lawley, B., Ripley, S., Bridge, P. & Convey, P. Molecular analysis of geographic patterns of eukaryotic diversity in antarctic soils. Appl. Environ. Microbiol. 70, 5963-5972 (2004).
19. 2 affects soil microbial diversity associated with trembling aspen. Environ. Microbiol. Rep. 10, 926-941 (2008).
20. Bailly, J. et al. Soil eukaryotic functional diversity, a metatranscriptomic approach. ISME J. 1, 632-642 (2007).
21. Bates, S. T. et al. Global biogeography of highly diverse protistan communities in soil. ISME J. 7, 652-659 (2013).
22. Baldwin, D. S. et al. Impacts of inundation and drought on eukaryote biodiversity in semi-arid floodplain soils. Mol. Ecol. 22, 1746-1758 (2013).
23. Urich, T. et al. Simultaneous assessment of soil microbial community structure and function through analysis of the metatranscriptome. PLoS ONE 3, e2527 (2008).
24. Tveit, A., Schwacke, R., Svenning, M. M. & Urich, T. Organic carbon transformations in high-Arctic peat soils: key functions and microorganisms. ISME J. 7, 299-311 (2013).
25. Stephenson, S. L., Schnittler, M. & Novozhilov, Y. Myxomycete diversity and distribution from the fossil record to the present. Biodiv. Conserv. 17, 285-301 (2008).
26. Page, F. C. The classification of "naked" amoebae (Phylum Rhizopoda). Arch. Protistenkd. 133, 199-217 (1987).
27. Kamono, A. & Fukui, M. Rapid PCR-based method for detection and differentiation of Didymiaceae and Physaraceae (Myxomycetes) in environmental samples. J. Microbiol. Methods 67, 496-506 (2006).
28. Kamono, A., Matsumoto, J., Kojima, H. & Fukui, M. Characterization of myxomycete communities in soil by reverse transcription polymerase chain reaction (RT-PCR)-based method. Soil Biol. Biochem. 41, 1324-1330 (2009).
29. Kamono, A., Meyer, M., Cavalier-Smith, T., Fukui, M. & Fiore-Donno, A. M. Exploring slime mould diversity in high-altitude forests and grasslands by environmental RNA analysis. FEMS Microbiol. Ecol. 94, 98-109 (2013).
30. Win Ko Ko, T., Stephenson, S. L., Jeewon, R. & Hyde, K. D. Molecular diversity of myxomycetes associated with decaying wood and forest floor leaf litter. Mycologia 101, 592-598 (2009).
31. Kamono, A., Kojima, H., Matsumoto, J., Kawamura, K. & Fukui, M. Airborne myxomycete spores: detection using molecular techniques. Naturwissenschaften 96, 147-151 (2009).
32. Fiore-Donno, A. M. et al. 18S rDNA phylogeny of Lamproderma and allied genera (Stemonitales, Myxomycetes, Amoebozoa). PLoS ONE 7, e35359 (2012).
33. Fiore-Donno, A. M. et al. Deep phylogeny and evolution of slime moulds (Mycetozoa). Protist 161, 55-70 (2010).
34. Fiore-Donno, A. M., Novozhilov, Y., Meyer, M. & Schnittler, M. Genetic structure of two protist species (Myxogastria, Amoebozoa) suggests asexual reproduction in sexual amoebae. PLoS ONE 6, e22872 (2011).
35. Nandipati, S. C., Haugli, K., Coucheron, D. H., Haskins, E. F. & Johansen, S. Polyphyletic origin of the genus Physarum (Physarales, Myxomycetes) revealed by nuclear rDNA mini-chromosome analysis and group I intron synapomorphy. BMC Evol. Biol. (2012).
36. Geisen, S., Fiore-Donno, A. M., Walochnik, J. & Bonkowski, M. Acanthamoeba everywhere: high diversity of Acanthamoeba in soils. Parasitol. Res. 113, 3151-3158 (2014).
37. Pussard, M. & Pons, R. Morphologie de la paroi kystique et taxonomie du genre Acanthamoeba (Protozoa, Amoebida). Protistologica 8, 557-598 (1977).
38. Stothard, D. R. et al. The evolutionary history of the genus Acanthamoeba and the identification of eight new 18s rRNA gene sequence types. J. Euk. Microbiol. 45, 45-54 (1998).
39. Risler, A., Coupat-Goutaland, B. & Pélandakis, M. Genotyping and phylogenetic analysis of Acanthamoeba isolates associated with keratitis. Parasitol. Res. 112, 3807-3816 (2013).
40. Qvarnstrom, Y., Nerad, T. A. & Visvesvara, G. S. Characterization of a new pathogenic Acanthamoeba species, A. byersi n. sp., isolated from a human with fatal amoebic encephalitis. J. Euk. Microbiol. (2013).
41. Fontes Landell, M., Salton, J., Caumo, K., Broetto, L. & Rott, M. B. Isolation and genotyping of free-living environmental isolates of Acanthamoeba spp. from bromeliads in Southern Brazil. Exp. Parasitol. 134, 290-294 (2013).
42. Corsaro, D. & Venditti, D. More Acanthamoeba genotypes: Limits to the use of rDNA fragments to describe new genotypes. Acta Protozool. 50, 49-54 (2011).
43. Gast, R. J., Ledee, D. R., Fuerst, P. A. & Byers, T. J. Subgenus systematics of Acanthamoeba: Four nuclear 18S rDNA sequence types. J. Euk. Microbiol. 43, 498-504 (1996).
44. Fischer, M. et al. Implementing largescale and longterm functional biodiversity research: The Biodiversity Exploratories. Basic and Applied Ecology 11, 473-485 (2010).
45. Reeder, J. & Knight, R. The "rare biosphere": a reality check. Nat. Meth. 6, 636-637 (2009).
46. Almeida-Neto, M., Guimarães, P., Guimarães, P. R., Jr, Loyola, R. D. & Ulrich, W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227-1239 (2008).
47. Bonkowski, M. & Clarholm, M. Stimulation of plant growth through interactions of bacteria and protozoa: testing the auxiliary microbial loop hypothesis. Acta Protozool. 51, 237-247 (2012).
48. Krome, K. et al. Soil bacteria and protozoa affect root branching via effects on the auxin and cytokinin balance in plants. Plant Soil 328, 191-201 (2010).
49. Rosenberg, K. et al. Soil amoebae rapidly change bacterial community composition in the rhizosphere of Arabidopsis thaliana. ISME J. 3, 675-684 (2009).
50. Ing, B. The phytosociology of myxomycetes. New Phytol. 126, 175-201 (1994).
51. Feest, A. & Madelin, M. F. Numerical abundance of myxomycetes (myxogastrids) in soils in the West of England. FEMS Microbiol. Ecol. 31, 353-360 (1985).
52. Feest, A. & Madelin, M. F. Seasonal population changes of myxomycetes and associated organisms in five non-woodland soils, and correlations between their numbers and soil characteristics. FEMS Microbiol. Ecol. 53, 141-152 (1988).
53. Howard, F. & Currie, M. Parasitism of myxomycete plasmodia on fungous mycelia. J. Arnold Arb. 13, 438-447 (1932).
54. Domonell, A., Brabender, M., Nitsche, F., Bonkowski, M. & Arndt, H. Community structure of cultivable protists in different grassland and forest soils of Thuringia. Pedobiologia 56, 1-7 (2013).
55. Stephenson, S. L., Fiore-Donno, A. M. & Schnittler, M. Myxomycetes in soil. Soil Biol. Biochem. 43, 2237-2242 (2011).
56. Madelin, M. F. Methods for studying the ecology and population dynamics of soil myxomycetes. Meth. Microbiol. 22, 405-416 (1990).
57. Feest, A. & Madelin, M. F. A method for the enumeration of myxomycetes in soils and its application to a wide range of soils. FEMS Microbiol. Ecol. 31, 103-109 (1985).
58. Clark, J. & Haskins, E. F. Reproductive systems in the myxomycetes: a review. Mycosphere 1, 337-353 (2010).
59. Booton, G. C., Visvesvara, G. S., Byers, T. J., Kelly, D. J. & Fuerst, P. A. Identification and distribution of Acanthamoeba species genotypes associated with nonkeratitis infections. J. Clin. Microbiol. 43, 1689-1693 (2005).
60. Kong, H. H. Molecular phylogeny of Acanthamoeba. Korean J. Parasitol. 47, S21-S28 (2009).
61. Caron, D. A. & Countway, P. D. Hypotheses on the role of the protistan rare biosphere in a changing world. Aquat. Microb. Ecol. 57, 227-238 (2009).
62. McGill, B. J. et al. Species abundance distributions: moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett. 10, 995-1015 (2007).
63. Foissner, W. Biogeography and dispersal of micro-organisms: a review emphasizing protists. Acta Protozool. 45, 111-136 (2006).
64. Schloss, P. D. et al. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75, 7537-7541 (2009).
65. Niu, B., Fu, L., Sun, S. & Li, W. Artificial and natural duplicates in pyrosequencing reads of metagenomic data. BMC Bioinf. 11 (2010).
66. Altschul, S. F. et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl. Ac. Res. 25, 3389-3402 (1997).
67. Hall, T. A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95-98 (1999).
68. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772-780 (2013).
69. Schloss, P. D. The effects of alignment quality, distance calculation method, sequence filtering, and region on the analysis of 16S rRNA gene-based studies. PLoS Comp. Biol. 6, e1000844 (2010).
70. Fonseca, V. et al. Sample richness and genetic diversity as drivers of chimera formation in nSSU metagenetic analyses. Nucl. Ac. Res. 40, e66 (2012).
71. Edgar, R., Haas, B., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed for chimera detection. Bioinformatics 27, 2194-2200 (2011).
72. Huse, S. M., Welch, D. M., Morrison, H. G. & Sogin, M. Ironing out the wrinkles in the rare biosphere through improved OTU clustering. Environ. Microbiol. Rep. 12, 1889-1898 (2010).
73. Quince, C. et al. Accurate determination of microbial diversity from 454 pyrosequencing data. Nat. Meth. 6, 639-641 (2009).
74. Kunin, V., Engelbrektson, A., Ochman, H. & Hugenholtz, P. Wrinkles in the rare biosphere: pyrosequencing errors can lead to artificial inflation of diversity estimates. Environ. Microbiol. Rep. 12, 118-123 (2010).
75. Johansen, T., Johansen, S. & Haugli, F. B. Nucleotide sequence of Physarum polycephalum small subunit ribosomal RNA as inferred from the gene sequence: secondary structure and evolutionary implications. Curr. Genet. 14, 265-273 (1988).
76. Bernhart, S. H., Hofacker, I. L., Will, S., Gruber, A. R. & Stadler, P. F. RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinf. 9, e474 (2008).
77. Guindon, S. & Gascuel, O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52, 696-704 (2003).
78. Baselga, A., Jiménez-Valverde, A. & Niccolini, G. A multiple-site similarity measure independent of richness. Biol. Lett. 3, 642-645 (2007).
79. Oksanen, J. et al. Vegan: Community Ecology Package. R package version 2.0-10. http://CRAN.R-project.org/package=vegan. (2013).
80. Strona, G., Galli, P., Seveso, D., Montano, S. & Fattorini, S. Nestedness for dummies (NeD): A user-friendly web interface for exploratory nestedness analysis. J. Stat. Softw. 59, 1-9 (2014).