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SSU rRNA reveals major trends in oomycete evolution

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Abstract

Oomycetes are a group of heterokonts that have a huge impact on the environment as well as on human welfare, due the parasitic nature of many species. However, their evolutionary patterns are still not well understood, due in part to the lack of molecular markers suited to resolve the deep phylogeny of this group. Here, we propose a phylogeny of the whole clade based on the nuclear ribosomal small subunit gene, that comprises both culture and environmental studies derived sequences. Our analysis shows notably that i) plant pathogenesis occurred only rarely in oomycete evolution in comparison to animal parasitism ii) obligate symbiosis happened only in a few derived groups and iii) transitions from soil/freshwater to marine environment (and viceversa) are common unlike for most eukaryotic groups. This study illustrates the complexity of evolutionary patterns and will help to better understand the emergence of pathogenicity in the different oomycete groups.

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References

  • Alverson AJ, Jansen RK, Theriot EC (2007) Bridging the Rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Mol Phylogenet Evol 45:193–210

    Article  PubMed  CAS  Google Scholar 

  • Bass D, Cavalier-Smith T (2004) Phylum-specific environmental DNA analysis reveals remarkably high global biodiversity of Cercozoa (Protozoa). Int J Syst Evol Microbiol 54:2393–2404

    Google Scholar 

  • Beakes GW (1981) Ultrastructural aspects of oospore differentiation. In: Hohl HR, Turian G (eds) The fungal spore: morphogenetic controls. Academic Press, London and New York, pp 71–94

    Google Scholar 

  • Beakes GW, Sekimoto S (2009) The evolutionary phylogeny of Oomycetes—insights gained from studies of holocarpic parasites of algae and invertebrates. In: Lamour K, Kamoun S (eds) Oomycete genetics and genomics: diversity, interactions, and research tools. Wiley-Blackwell, London, pp 1–24

    Chapter  Google Scholar 

  • Ben Ali A, De Baere R, Van der Auwera G, De Wachter R, Van de Peer Y (2001) Phylogenetic relationships among algae based on complete large-subunit rRNA sequences. Int J Syst Evol Microbiol 51:737–749

    Article  PubMed  CAS  Google Scholar 

  • Ben Ali A, De Baere R, De Wachter R, Van de Peer Y (2002) Evolutionary relationships among heterokont algae (the autotrophic stramenopiles) based on combined analyses of small and large subunit ribosomal RNA. Protist 153:123–132

    Article  PubMed  CAS  Google Scholar 

  • Berney C, Fahrni J, Pawlowski J (2004) How many novel eukaryotic kingdoms? Pitfalls and limitations of environmental DNA surveys. BMC Biology 2:1–13

    Google Scholar 

  • Bessey EA (1942) Some problems in fungus phylogeny. Mycologia 34:355–379

    Google Scholar 

  • Brate J, Klaveness D, Rygh T, Jakobsen KS, Shalchian-Tabrizi K (2010a) Telonemia-specific environmental 18S rDNA PCR reveals unknown diversity and multiple marine-freshwater colonizations. BMC Microbiol 10:168

    Article  PubMed  Google Scholar 

  • Brate J, Logares R, Berney C, Ree DK, Klaveness D, Jakobsen KS, Shalchian-Tabrizi K (2010b) Freshwater Perkinsea and marine-freshwater colonizations revealed by pyrosequencing and phylogeny of environmental rDNA. ISME J 4:1144–1153

    Article  PubMed  CAS  Google Scholar 

  • Cavalier-Smith T, Chao EEY (2006) Phylogeny and megasystematics of phagotrophic heterokonts (kingdom Chromista). J Mol Evol 62:388–420

    Article  PubMed  CAS  Google Scholar 

  • Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate phenol chloroform extraction. Anal Biochem 162:156–159

    Article  PubMed  CAS  Google Scholar 

  • Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Microbiol 30:17–32

    Google Scholar 

  • Duran A, Gryzenhout M, Drenth A, Slippers B, Ahumada R, Wingfield BD, Wingfield MJ (2010) AFLP analysis reveals a clonal population of Phytophthora pinifolia in Chile. Fungal Biol 114:746–752

    Article  PubMed  Google Scholar 

  • Gachon CMM, Strittmatter M, Muller DG, Kleinteich J, Kupper FC (2009) Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Appl Environ Microbiol 75:322–328

    Article  PubMed  CAS  Google Scholar 

  • Glockling SL, Beakes GW (2006) An ultrastructural study of development and reproduction in the nematode parasite Myzocytiopsis vermicola. Mycologia 98:1–15

    Article  PubMed  Google Scholar 

  • Göker M, Voglmayr H, Riethmuller A, Oberwinkler F (2007) How do obligate parasites evolve? A multi–gene phylogenetic analysis of downy mildews. Fungal Genet Biol 44:105–122

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Ho HH, Chang HS, Hsieh SY (1991) Halophytophthora kandeliae, a new marine fungus from Taiwan. Mycologia 83:419–424

    Article  Google Scholar 

  • Holzmann M, Habura A, Hannah G, Bowser SS, Pawlowski J (2003) Freshwater foraminiferans revealed by analysis of environmental DNA samples. J Eukaryot Microbiol 50:135–139

    Google Scholar 

  • Hudspeth DSS, Nadler SA, Hudspeth MES (2000) A COX2 molecular phylogeny of the peronosporomycetes. Mycologia 92:674–684

    Article  CAS  Google Scholar 

  • Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18

    Article  PubMed  Google Scholar 

  • Kamoun S (2001) Nonhost resistance to Phytophthora: novel prospects for a classical problem. Curr Opin Plant Biol 4:295–300

    Article  PubMed  CAS  Google Scholar 

  • Kamoun S (2009). The secretome of plant-associated fungi and oomycetes. In 'Plant Relationships, 2nd Edition, The Mycota V' H. Deising (Ed.), Springer-Verlag Berlin Heidelberg

  • Karling JS (1942) The simple holocarpic biflagellate phycomycetes. Columbia University Press, New York

  • Lara E, Moreira D, López García P (2010) The environmental clade LKM11 and Rozella form the deepest branching clade of Fungi. Protist 161:116–121

  • Lara E, Mitchell EAD, Moreira D, López García P (2011) Highly diverse and seasonally dynamic protist community in a pristine peat bog. Protist 162:14–32

  • Logares R, Shalchian-Tabrizi K, Boltovskoy A, Rengefors K (2007) Extensive dinoflagellate phylogenies indicate infrequent marine-freshwater transitions. Mol Phylogenet Evol 45:887–903

    Article  PubMed  CAS  Google Scholar 

  • Ludwig-Köhn H, Jahnke KD, Bahnweg G (1982) Sterol composition and sterol metabolism of Haliphthoros milfordensis and Atkinsiella dubia, fungal parasites of marine crustaceans. Biochimica et Biophysica Acta (BBA) - Lipids and Lipid Metabolism 713:463–469

    Google Scholar 

  • Massana R, Castresana J, Balague V, Guillou L, Romari K, Groisillier A, Valentin K, Pedro-Alio C (2004). Phylogenetic and ecological analysis of novel marine stramenopiles. App Environ Microbiol 70:3528–3534

    Google Scholar 

  • Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA coding regions. Gene 71:491–499

    Article  PubMed  CAS  Google Scholar 

  • Mendoza L, Newton JC (2005) Immunology and immunotherapy of the infections caused by Pythium insidiosum. Med Mycol 43:477–486

    Article  PubMed  CAS  Google Scholar 

  • Moreira D, Lopez-Garcia P, Vickerman K (2004) An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. Int J Syst Evol Microbiol 54:1861–1875

    Article  PubMed  CAS  Google Scholar 

  • Petersen AB, Rosendahl S (2000) Phylogeny of the Peronosporomycetes (Oomycota) based on partial sequences of the large ribosomal subunit (LSU rDNA). Mycol Res 104:1295–1303

    Google Scholar 

  • Phillips AJ, Anderson VL, Robertson EJ, Secombes CJ, van West P (2008) New insights into animal pathogenic oomycetes. Trends Microbiol 16:13–19

    Article  PubMed  CAS  Google Scholar 

  • Riethmuller A, Voglmayr H, Goker M, Weiss M, Oberwinkler F (2002) Phylogenetic relationships of the downy mildews (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia 94:834–849

    Article  PubMed  Google Scholar 

  • Rizzo DM, Garbelotto M, Hansen EA (2005) Phytophthora ramorum: Integrative research and management of an emerging pathogen in California and Oregon forests. Annu Rev Phytopathol 43:309–335

    Article  PubMed  Google Scholar 

  • Rodriguez F, Oliver JL, Marin A, Medina JR (1990) The general stochastic-model of nucleotide substitution. J Theor Biol 142:485–501

    Article  PubMed  CAS  Google Scholar 

  • Shalchian-Tabrizi K, Brate J, Logares R, Klaveness D, Berney C, Jakobsen KS (2008) Diversification of unicellular eukaryotes: cryptomonad colonizations of marine and fresh waters inferred from revised 18S rRNA phylogeny. Environ Microbiol 10:2635–2644

    Article  PubMed  CAS  Google Scholar 

  • Sparrow FK (1976) The present status of classification in biflagellate fungi. In: Gareth-Jones EB (ed) Recent advances in aquatic mycology. Elek Science, London, pp 213–222

  • Stamatakis, A., Hoover, P. and Rougemont, J., (2008). A Rapid Bootstrap Algorithm for the RAxML Web Servers. Syst Biol 57(5):758–771

    Google Scholar 

  • Thines M, Kamoun S (2010) Oomycete-plant coevolution: recent advances and future prospects. Curr Opin Plant Biol 13:427–433

    Article  PubMed  Google Scholar 

  • Uzuhashi S, Tojo M, Kakishima M (2010) Phylogeny of the genus Pythium and description of new genera. Mycoscience 51:337–365

    Article  Google Scholar 

  • Van der Pläats-Niterink AJ (1981) Monograph of the genus Pythium. Studies in Mycology 21:1–242

    Google Scholar 

  • van West P, de Bruijn I, Minor KL, Phillips AJ, Robertson EJ, Wawra S, Bain J, Anderson VL, Secombes CJ (2010) The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiol Lett 310:127–137

    Article  PubMed  Google Scholar 

  • Wolinska J, Giessler S, Koerner H (2009) Molecular identification and hidden diversity of novel daphnia parasites from European Lakes. Appl Environ Microbiol 75:7051–7059

    Google Scholar 

  • Zattau WC, McInnis T (1987) Life-Cycle and mode of infection of Leptolegnia chapmanii (oomycetes) parasitizing Aedes aegypti. J Invertebr Pathol 50:134–145

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by the Swiss State Secretariat for Education and Research (grant reference: SER No. C09.0139) and the European Union for the projects ISEFOR “Increasing Sustainability of European Forests: Modelling for Security against Invasive Pests and Pathogens under Climate Change (FP7-KBBE-2009-3 call, Proposal number: 245268) and the COST action FP0801 “Established and Emerging Phytophthora: Increasing Threats to Woodland and Forest Ecosystems in Europe”. The authors would like to thank Mário Rui Proença Santos (Universidade Tecnica de Lisboa - Portugal) for the Albugo infected Brassica rapa plant material.

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Correspondence to Lassaad Belbahri.

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Lara, E., Belbahri, L. SSU rRNA reveals major trends in oomycete evolution. Fungal Diversity 49, 93–100 (2011). https://doi.org/10.1007/s13225-011-0098-9

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  • DOI: https://doi.org/10.1007/s13225-011-0098-9

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