Skip to main content

Advertisement

SpringerLink
Log in

New phylogenetic insights into Saprolegniales (Oomycota, Straminipila) based upon studies of specimens isolated from Brazil and Argentina

  • Original Article
  • Published:
Mycological Progress Aims and scope Submit manuscript

Abstract

Saprolegniales is a complex and monophyletic order of oomycetes. Their members inhabit terrestrial, freshwater, and marine ecosystems and have a worldwide distribution. In these ecosystems, they are found as saprobes, parasites, or even pathogens of animals and plants of economic importance. In this study, a concatenate phylogeny of the partial LSU and complete ITS rDNA regions is presented, including isolates from Brazil and Argentina, which were sequenced after a detailed morphological analysis. Among the sequenced species, Achlya orion, Leptolegnia eccentrica, Phragmosporangium uniseriatum, and Pythiopsis irregularis are included for the first time in a phylogeny. Our results are in agreement with the recent informal proposals outlined in taxonomic overviews of the Oomycota of G.W. Beakes and collaborators, who placed the family Verrucalvaceae into the Saprolegniales and introduced the family Achlyaceae to group Achlya s.s., Brevilegnia, Dictyuchus, and Thraustotheca. These results also support the transference of Achlya androgyna to Newbya. Leptolegnia appears as paraphyletic, with the separation of L. eccentrica from the other species of this genus. In addition, Phragmosporangium, which is herein sequenced for the first time, clustered as sister to some species of Aphanomyces, including the type species, A. stellatus.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ault KK, Johnson JE, Pinkart HC, Wagner RS (2012) Genetic comparison of water molds from embryos of amphibians Rana cascadae, Bufo boreas and Pseudacris regilla. Dis Aquat Org 99:127–137

    Article  PubMed  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. John Wiley & Sons, Inc., United States, pp 1–24

    Google Scholar 

  • Beakes GW, Thines M (2017) Hyphochytriomycota and Oomycota. In: Archibald J, Simpson A, Slamovits C (eds) Handbook of the Protists. Springer International Publishing, Cham, pp 435–505

    Chapter  Google Scholar 

  • Beakes GW, Honda D, Thines M (2014a) Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota. In: McLaughlin DJ, Spatafora JW (eds) the Mycota VIII part a. Springer-Verlag, Berlin/Heidelberg, pp 39–97

    Google Scholar 

  • Beakes GW, Glockling SL, James TY (2014b) A new oomycete species parasitic in nematodes, Chlamydomyzium dictyuchoides sp. nov.: developmental biology and phylogenetic studies. Fungal Biol 118:527–543

    Article  PubMed  Google Scholar 

  • Beneke ES, Rogers AL (1962) Aquatic Phycomycetes isolated in the states of Minas Gerais, São Paulo and Paraná, Brazil. Rickia 1:181–193

    Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Dick MW, Vick MC, Gibbings JG, Hederson TA, Lopez-Lastra CC (1999) 18 S rDNA for species of Leptolegnia and other Peronosporemycetes: justification for the subclass taxa Saprolegniomycetidae and Peronosporomycetidae and division the Saprolegniaceae sensu lato into the families Leptolegniaceae and Saprolegniaceae. Mycol Res 103:1119–1125

    Article  CAS  Google Scholar 

  • Diéguez-Uribeondo J, Cerenius L, Dykova I, Gelder SR, Hentonen P, Jiravanichpaisal P, Lom J, Söderhäll K (2006) Pathogens, parasites and ectocommensals. In: Atlas of crayfish in Europe: distribution and diseases. Publications Scientifiques du Muséum national d'Histoire Naturelle. Patrimoines Naturels 64:135–155

    Google Scholar 

  • Diéguez-Uribeondo J, Fregeneda-Grandes JM, Cerenius L, Pérez-Iniesta E, Aller-Gancedo JM, Tellería MT, Söderhäll K, Martín MP (2007) Re-evaluation of the enigmatic species complex Saprolegnia diclina-Saprolegnia parasitica based on morphological, physiological and molecular data. Fungal Genet Biol 44:85–601

    Article  CAS  Google Scholar 

  • Diéguez-Uribeondo J, Garcia MA, Cerenius L, Kozúbiková E, Ballesteros I, Windels C, Weiland J, Kator H, Sorderhall K, Martín MP (2009) Phylogenetic relationships among plant and animal parasites, and saprotrophs in Aphanomyces (oomycetes). Fungal Genet Biol 46:365–376

    Article  PubMed  CAS  Google Scholar 

  • Fernández-Benéitez MJ, Ortiz-Santaliestra ME, Lizana M, Diéguez-Uribeondo J (2007) Saprolegnia diclina: another species responsible for the emergente disease ‘Saprolegnia infections’ in amphibians. FEMS Microbiol 279:23–29

    Article  CAS  Google Scholar 

  • Gaulin E, Jacquet C, Bottin A, Dumas B (2007) Root rot disease of legumes caused by Aphanomyces euteiches. Mol Plant Pathol 8:539–548

    Article  PubMed  Google Scholar 

  • Gleason FH, Chambouvet A, Sullivan BK, Lilje O, Rowley JJL (2014) Multiple zoosporic parasites pose a significant threat to amphibian populations. Fungal Ecol 11:181–192

    Article  Google Scholar 

  • Gonçalves DR, Rocha SCO, Pires-Zottarelli CLA (2017) Protoachlya papillata (Saprolegniales, Oomycota): a new name for Protoachlya hypogyna (Coker & Pemberton) TW Johnson & RL Seym. Phytotaxa 314:273–278

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:679–704

    Article  Google Scholar 

  • Hulvey J, Padgett DE, Bailey JC (2007) Species boundaries within Saprolegnia (Saprolegniales, Oomycota) based on morphological and DNA sequence data. Mycologia 99:421–429

    Article  PubMed  CAS  Google Scholar 

  • Jerônimo GH, de Jesus AL, SCO R, Gonçalves DR, Pires-Zottarelli CLA (2017) New insights into Plectospira genus (oomycetes, Straminipila): morphological and molecular analyses. Phytotaxa 307:191–198

    Article  Google Scholar 

  • Jesus AL, Marano AV, de Souza JI, James TY, Jerônimo GH, Rocha SCO, Gonçalves DR, Boro MC, Pires-Zottarelli CLA (2015) Achlya catenulata sp. nov., a new Saprolegniales (oomycetes, Straminipila) from Brazilian mangrove swamp. Phytotaxa 212:221–228

    Article  Google Scholar 

  • Johnson Jr TW, Seymour RL, Padget DE, (2002) Biology and systematic of the Saprolegniaceae. http://dl.uncw.edu/digilib/biology/fungi/taxonomy%20and%20systematics/padgett%20book, acessed in 26 December 2017

  • Johnson TW Jr, Seymour RL, Padgett DE (2005a) Systematics of the Saprolegniaceae: new combination. Mycotaxon 92:11–32

    Google Scholar 

  • Johnson TW Jr, Seymour RL, Padgett DE (2005b) Systematics of the Saprolegniaceae: new taxa. Mycotaxon 92:1–10

    Google Scholar 

  • Kazutaka K, Daron MS (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772−780

    Google Scholar 

  • Kiziewicz B, Diéguez-Umberondo J, Martin MP (2013) Water Saprolegnia diclina (FLO) isolated from eggs of Carassius carassius L. in Bialystok rivers, Poland. Afr J Microbiol Res 7:5406–5410

    Article  Google Scholar 

  • Kozubíková E, Filipova L, Kozak P, Duris Z, Martín M, Diéguez-Uribeondo J, Oidtmann B, Petrusek A (2009) Prevalence of the crayfish plague pathogen Aphanomyces astaci in invasive American crayfishes in the Czech Republic. Conserv Biol 23:1204–1213

    Article  PubMed  Google Scholar 

  • Leclerc MC, Guillot J, Deville M (2000) Taxonomic and phylogenetic analysis of Saprolegniaceae (oomycetes) inferred from LSU rDNA and ITS sequence comparisons. Antonie Van Leeuwenhoek 77:369–377

    Article  PubMed  CAS  Google Scholar 

  • Madoui MA, Bertrand-Michel J, Gaulin E, Dumas B (2009) Sterol metabolism in the oomycete Aphanomyces euteiches, a legume root pathogen. New Phytol 183:291–300

    Article  PubMed  Google Scholar 

  • Maia LC, De Carvalho AA Jr, Cavalcanti LH, Gugliotta AM, Drechsler-Santos ER, Santiago ALMA, Cáceres EMES, Gibertoni TB, Aptroot A, Giachini AJ, Soares AMS, Silva ACG, Magnago AC, Goto BT, de Liras CRS, Montoya CAS, Pires-Zottarelli CLA, da Silva DKA, Soares DJ, Rezende DHC, Luz EDMN, Gumboski EL, Wartchow F, Karstedt F, Freire FM, Coutinho FP, de Melo GSN, Sotão HMP, Baseia IG, Pereira J, de Oliveira JJS, Souza JF, Bezerra JL, Neta LSA, Pfenning LH, Gusmão LFP, Neves MA, Capelari M, Jaeger MC, Pulgarín MP, Junior NM, de Medeiros PS, Friedrich RCS, Chikowskiv RS, Pires RP, Melo RF, de Silveira RMB, Urrea-Valencia S, Cortez VG, da Silva VF (2015) Diversity of Brazilian fungi. Rodriguésia 66:1033–1045

    Article  Google Scholar 

  • Marano AV, Jesus AL, de Souza JI, Leãno EM, James TY, Jerônimo GH, de Cock AWAM, Pires-Zottarelli CLA (2014) A new combination in Phytopythium: P. kandeliae (oomycetes, Straminipila). Mycosphere 5:510–522

    Article  Google Scholar 

  • Marano AV, Gleason FH, Rocha SCO, Pires-Zottarelli CLA, de Souza JI (2017) Crown oomycetes have evolved as effective plant and animal parasites. In: Dighton J, White JF (eds) The fungal community. CRC Press, United States, pp 257–272

    Chapter  Google Scholar 

  • Mastan SA (2015) Fungal infection in freshwater fishes of Andhra Pradesh, India. Afr J Biotechnol 14:530–534

    Article  Google Scholar 

  • Miranda ML, Pires-Zottarelli CLA (2012) Oomicetos do Parque Estadual da Serra da Cantareira, São Paulo, SP, Brasil. Hoehnea 39:95–112

    Article  Google Scholar 

  • Molloy DP, Glockling SL, Siegfried CA, Gordon W, Beakes GW, James TY, Mastitsky SE, Wurdak E, Giamberini L, Gaylo MJ, Michael J, Nemeth MJ (2014) Aquastella gen. nov.: a new genus of saprolegniaceous oomycete rotifer parasites related to Aphanomyces, with unique sporangial outgrowths. Fungal Biol 118:544–558

    Article  PubMed  Google Scholar 

  • Nascimento CA, Pires-Zottarelli CLA (2012) Diversidade de fungos zoospóricos da Reserva Biológica de Mogi Guaçu, estado de São Paulo, Brasil. Rodriguésia 63:587–611

    Article  Google Scholar 

  • Noga EJ (2010) Fish disease: diagnosis and treatment, 2nd edn. John Wiley and Sons, United States

    Book  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pires-Zottarelli CLA, Michelin F (2012) Fungos zoospóricos da Serra do Itapeti. In: Serra do Itapeti: Aspectos históricos, sociais e naturalísticos. In: Morini MSC, Miranda VFO (eds) Canal 6 editora. Bauru, pp 155–166

  • Pires-Zottarelli CLA, Gomes AL, de Oliveira JM, Milanez AI (2007) Phragmosporangium uniseriatum in Brazil. Mycotaxon 102:179–182

    Google Scholar 

  • Rezinciuc S, Sandoval-Sierra JV, Dieguez-Uribeondo J (2014) Molecular identification of a bronopol tolerant strain of Saprolegnia australis causing egg and fry mortality in farmed brown trout, Salmo trutta. Fungal Biol 118:591–600

    Article  PubMed  CAS  Google Scholar 

  • Rezinciuc S, Sandoval-Sierra JV, Oidtmann B, Diéguez-Uribeondo J (2016) The biology of crayfish plague pathogen Aphanomyces astaci. Current answers to most frequent questions. In: Kawai T, Faulkes Z, Scholtz G (eds) Freshwater crayfish: a global overvie. CRC Press, Germany, pp 182–204

    Google Scholar 

  • Riethmüller A, Weiss M, Oberwinkler F (1999) Phylogenetic studies of Saprolegniomycetidae and related groups based on nuclear large subunit ribosomal DNA sequences. Can J Bot 77:1790–1800

    Article  Google Scholar 

  • Riethmüller A, Voglmayr H, Göker M, Weiβ 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 

  • Robideau GP, de Cock AWAM, Coffey MD, Voglmayr H, Brouwer H, Bala K, Chitty DW, Désaulniers N, Eggertson QA, Gachon CMM, Hu CH, Küpper FC, Rintoul TL, Sarhan E, Verstappen ECP, Zhang Y, Bonants PJM, Ristaino JB, Lévesque AC (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol Ecol Resour 11:1002–1011

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rocha SCO, Sandoval-Sierra JV, Diéguez-Uribeondo J, Gonçalves DR, Jerônimo GH, Jesus AL, Marano AV, Pires-Zottarelli CLA (2016a) Saprolegnia milanezii sp. nov., a new species of Saprolegniales (Oomycota, Straminipila) from Brazil. Phytotaxa 270:286–294

    Article  Google Scholar 

  • Rocha SCO, Jerônimo GH, Marano AV, de Souza JI, de Jesus AL, Pires-Zottarelli CLA (2016b) Oomycota from “Parque Estadual da Ilha do Cardoso” (PEIC): first records for São Paulo State and Brazil. Cryptogamie Mycol 37:1–15

    Google Scholar 

  • Romansic JM, Diez KA, Higashi EM, Johnson JE, Blaustein AR (2009) Effects of the pathogenic water mold Saprolegnia ferax on survival of amphibian larvae. Dis Aquat Org 83:187–193

    Article  PubMed  Google Scholar 

  • Sandoval-Sierra JV, Diéguez-Uribeondo J (2015) A comprehensive protocol for improving the description of saprolegniales (Oomycota): two practical examples (Saprolegnia aenigmatica sp. nov. and Saprolegnia racemosa sp. nov.) PLoS One 10:e0132999

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sandoval-Sierra JV, Latif-Eugenin F, Martín MP, Zaror L, Diéguez-Uribeondo J (2014a) Saprolegnia species affecting the salmonid aquaculture in Chile and their associations with fish developmental stage. Aquaculture 434:462–469

    Article  Google Scholar 

  • Sandoval-Sierra JV, Martín MP, Diéguez-Uribeondo J (2014b) Species identification in the genus Saprolegnia (oomycetes): defining DNA-based molecular operational taxonomic units. Fungal Biol 118:559–578

    Article  PubMed  CAS  Google Scholar 

  • Sarowar MN, Saraiva M, Jessop CN, Lilje O, Gleason FH, van West P (2014) Infection strategies of pathogenic oomycetes in fish. In: Jones KDG, Hyde KL, Pang EB (eds) Freshwater fungi and fungal-like organisms. Walter de Gruyter GmbH, Germany, pp 217–243

    Google Scholar 

  • Söderhäll K, Cerenius L (1999) The crayfish plague fungus: history and recent advances. Freshwater Crayfish 12:11–35

    Google Scholar 

  • Spencer MA, Vick MC, Dick MW (2002) Revision of Aplanopsis, Pythiopsis, and ‘subcentric’ Achlya species (Saprolegniaceae) using 18S rDNA and morphological data. Mycol Res 106:549–560

    Article  CAS  Google Scholar 

  • Steciow MM, Milanez AI, Pires-Zottarelli CLA, Marano AV, Letcher PM, Vélez CG (2012) Zoosporic true fungi, heterotrophic straminipiles and plasmodiophorids: status of knowledge in South América. Darwin 50:25–32

    Google Scholar 

  • Steciow MM, Lara E, Pillonel A, Pelizza SA, Lestani EA, Rossi GC, Belbahri L (2013) Incipient loss of flagella in the genus Geolegnia: the emergence of a new clade within Leptolegnia? IMA Fungus 4:169–175

    Article  PubMed  PubMed Central  Google Scholar 

  • Steciow MM, Lara H, Paul C, Pillonel A, Belbahri L (2014) Multiple barcode assessment within the Saprolegnia-Achlya clade (Saprolegniales, Oomycota, Straminipila) brings order in a neglected group of pathogens. IMA Fungus 5:439–448

    Article  PubMed  PubMed Central  Google Scholar 

  • Strand DA, Jussila J, Viijamaa-Dirks S, Kokko H, Makkonen J, Holst-Jensen A, Viljugrein H, Istad TV (2012) Monitoring the spore dynamics of Aphanomyces astaci in the ambient water of latent carrier crayfish. Vet Microbiol 160:99–107

    Article  PubMed  Google Scholar 

  • Unestam (1965) Studies on the crayfish plague fungus Aphanomyces astaci I. Some factors affecting growth in vitro. Physiol Plan 18:483–505

    Article  Google Scholar 

  • Urban MC, Lewis LA, Fučíková K, Cordone A (2015) Population of origin and environment interact to determine oomycete infections in spotted salamander populations. Oikos 124:274–284

    Article  Google Scholar 

  • Van den Berg AH, McLaggan D, Diéguez-Uribeondo J, Van West P (2013) The impact of the water moulds Saprolegnia diclina and Saprolegnia parasitica on natural ecosystems and the aquaculture industry. Fungal Biol 27:33–42

    Article  Google Scholar 

Download references

Acknowledgements

We wish to thank FAPESP (“Fundação de Amparo à Pesquisa do Estado de São Paulo”) for the financial support (Process 12/50222-7) and the scholarship given to SCO Rocha (Process 2014/04375-1). CNPq (“Conselho Nacional de Desenvolvimento Científico e Tecnológico”) is also knowledged for the fellowship given to CLA Pires-Zottarelli (Process 304411/2012-4). Finally, we thank the anonymous reviewers and the editor Marco Thines for their relevant contributions.

Author information

Authors and Affiliations

  1. Instituto de Botânica, Núcleo de Pesquisa em Micologia, Av. Miguel Estefano 3687, CEP, São Paulo, SP, 04301-012, Brazil

    Sarah C. O. Rocha, Agostina V. Marano, José I. de Souza & Carmen L. A. Pires-Zottarelli

  2. Centro de Estudios Parasitologicos y de Vectores, La Plata, Buenos Aires, Argentina

    Claudia C. Lopez-Lastra & Manuel E. Rueda-Páramo

Authors
  1. Sarah C. O. Rocha
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Claudia C. Lopez-Lastra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Agostina V. Marano
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. José I. de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel E. Rueda-Páramo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Carmen L. A. Pires-Zottarelli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Sarah C. O. Rocha.

Additional information

Section Editor: Marco Thines

José Ivanildo de Souza is deceased.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Rocha, S.C.O., Lopez-Lastra, C.C., Marano, A.V. et al. New phylogenetic insights into Saprolegniales (Oomycota, Straminipila) based upon studies of specimens isolated from Brazil and Argentina. Mycol Progress 17, 691–700 (2018). https://doi.org/10.1007/s11557-018-1381-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11557-018-1381-x

Keywords

Search

Navigation