Skip to main content
Log in

Morphological and phylogenetic analyses of Saprolegniales (Oomycota) reveal taxonomic and nomenclatural novelties

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

Abstract

Saprolegniaceae s.l. is a species-rich family of the monophyletic order Saprolegniales (Oomycota, Straminipila). Members of this family are primarily saprotrophs on cellulosic, chitinous, and proteinaceous materials in both aquatic and terrestrial ecosystems. This family also includes pathogens infecting various hosts, such as plants, crustaceans, and fishes at various life cycle stages. A diversity survey of Saprolegniaceae s.l. from freshwater and soil of the Brazilian Atlantic Rainforest resulted in 20 species isolated and identified through morphological and molecular analyses. These analyses revealed two new genera (Beakesia and Cokeria) and two new species, Achlya delicata and Brevilegnia milaneziana. Beakesia is proposed to accommodate Achlya catenulata, while Cokeria includes species with subcentric and centric oospores previously assigned to Achlya (A. racemosa, A. radiosa, and A. sparrowii). Our findings highlight the importance of additional sampling and studies in biodiversity-rich areas such as the Brazilian Atlantic Rainforest. They also provide a new perspective on the evolutionary relationships and nomenclatural delineation of traditional Oomycota genera, and revisit the family subdivisions of Saprolegniales, formally introducing Achlyaceae.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The full text of the manuscript will be available in Mycological Progress, the sequences at GenBank, and the specimens in the Herbarium SP and the CCIBt Culture Collection.

References

  • Beakes GW, Honda D, Thines M (2014) Systematics of the Straminipila: Labyrinthulomycota, Hyphochytriomycota, and Oomycota. In: McLaughlin DJ, Spatafora JW (eds) The Mycota VIII, Part A: Systematic and Evolution. Springer-Verlag, Berlin, pp 39–97. https://doi.org/10.1007/978-3-642-55318-9_3

  • 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. https://doi.org/10.1007/978-3-319-32669-6_26-1

  • 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 

  • Beneke ES, Rogers AL (1970) Aquatic fungi of Parque Nacional do Itatiaia in the State of Rio de Janeiro. Rickia 5:51–64

    Google Scholar 

  • Choi YJ, Lee SH, Nguyen TTT, Nam B, Lee HB (2019) Characterization of Achlya americana and A. bisexualis (Saprolegniales, Oomycota) isolated from freshwater environments in Korea. Mycobiology 47:135–142. https://doi.org/10.1080/12298093.2018.1551855

    Article  PubMed  PubMed Central  Google Scholar 

  • Coker WC (1923) The Saprolegniaceae with notes on other water molds, 1st edn. University North Carolina Press, United States

  • Czeczuga B, Bartel R, Kiziewicz B, Godlewska A, Muszyńska E (2005) Zoosporic Fungi growing on the eggs of sea trout (Salmo trutta m. trutta L.) in river water of varied trophicity. Pol J Environ Stud 3:295–303

    Google Scholar 

  • Czeczuga B, Czeczuga-Semniuk E, Semniuk-Grell A (2015) Observations of mycotal species growth on the rainbow trout eggs (Oncorhynchus mykiss). Afr J Microbiol Res 9:515–520. https://doi.org/10.5897/AJMR2014.7260

    Article  Google Scholar 

  • Czeczuga B, Godlewska A, Mazalska B, Muszyńska E (2010) Straminipilous organisms growing on herbivorous pirapitinga (Piaractus brachypomus) and carnivorous piranha (Pygocentrus nattereri) from Poland. Braz J Biol 2:335–339. https://doi.org/10.1590/S1519-69842010000200015

    Article  Google Scholar 

  • Czeczuga B, Kozlowska M, Godlewska A (2002) Zoosporic aquatic fungi growing on dead specimens of 29 freshwater crustacean species. Limnologica 32:180–193. https://doi.org/10.1016/S0075-9511(02)80007-X

    Article  CAS  Google Scholar 

  • Dick MW (2001) Straminipilous fungi. Kluwer Academic Publishers, Dordrecht. https://doi.org/10.1007/978-94-015-9733-3

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

    Article  CAS  Google Scholar 

  • Engblom C, Landor L, Sjöqvist C, Korkea-aho T, Viljamaa-Dirks S, Paulin L, Wiklund T (2023) Identification and genetic characterization of Saprolegnia parasitica, isolated from farmed and wild fish in Finland. J Fish Dis 46:849–860

    Article  CAS  PubMed  Google Scholar 

  • Godlewska A, Kiziewicz B, Muszyńska E, Mazalska B (2009) Fungi and straminipilous organisms found in ponds in Białystok. Pol J Environ Stud 18:369–376

    CAS  Google Scholar 

  • Indoh H (1941) Observations on some aquatic moulds collected from Micronesia (preliminary note). Nat Hist (Tokyo) 38:86–91

    Google Scholar 

  • Jerônimo GH, Jesus AJ, Rocha SCO, Gonçalves DR, Pires-Zottarelli CLA (2017) New insights into Plectospira genus (Oomycetes, Straminipila): morphological and molecular analyses. Phytotaxa 307:191–198. https://doi.org/10.11646/phytotaxa.307.3.3

  • Jerônimo GH, Pires-Zottarelli CLA (2020) Morphological and phylogenetic study of Oomycetes in three tropical reservoirs. Sydowia 73:31–44. https://doi.org/10.12905/0380.sydowia73-2020-0031

  • Jesus AL, Gonçalves DR, Rocha SCO, Marano AV, Jerônimo GH, de Souza JI, Boro MC, Pires-Zottarelli CLA (2016) Morphological and phylogenetic analyses of three Phytopythium species (Peronosporales, Oomycota) from Brazil. Cryptogamie, Mycol 37:1–12. https://doi.org/10.7872/crym/v37.iss1.2016.117

    Article  Google Scholar 

  • Jesus AL, Marano AV, Schoenlein-Crusius IH, Pires-Zottarelli CLA (2013) Diversidade de organismos zoospóricos do córrego Pirarungaua, Parque Estadual das Fontes do Ipiranga, São Paulo, Brasil: novas citações. Hoehnea 40:167–180. https://doi.org/10.1590/S2236-89062013000100009

    Article  Google Scholar 

  • Jesus AL, Marano AL, de Souza J, 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. https://doi.org/10.11646/phytotaxa.212.3.4

  • Johnson Jr TW, Seymour RL, Padgett DE (2002) Biology and systematics of Saprolegniaceae. Available from: http://people.uncw.edu/padgett/book/READ_FIRST/Preface.pdf. Accessed 30 April 2021

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kück P, Mayer C, Wägele JW, Misof B (2012) Long branch effects distort maximum likelihood phylogenies in simulations despite selection of the correct model. PLoS ONE 7:e36593. https://doi.org/10.1371/journal.pone.0036593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leclerc MC, Guillot J, Deville M (2000) Taxonomic and phylogenetic analyses of Saprolegniaceae (Oomycetes) inferred from LSU rDNA and ITS sequence comparisons. Anton Leeuw 77:369–377. https://doi.org/10.1023/a:1002601211295

    Article  CAS  Google Scholar 

  • Lyra NP, Milanez AI (1974) Notas para o levantamento dos ficomicetos aquáticos do Estado de São Paulo. Recife, Instituto de Micologia da Universidade Federal de Pernambuco, Publicação 698:1–27

  • Masigol H, Khodaparast SA, Mostowfizadeh-Ghalamfarsa R, Rojas-Jimenez K, Woodhouse JN, Neubauer D, Grossart H (2020) Taxonomical and functional diversity of Saprolegniales in Anzali lagoon, Iran. Aquat Ecol 54:323–336. https://doi.org/10.1007/s10452-019-09745-w

    Article  CAS  Google Scholar 

  • Masigol H, Van West P, Taheri SR, Fregeneda-Grandes J, Pârvulescu L, Mclaggan D, Bliss TT, Mostowfizadeh-Ghalamfarsa R, Pourmoghaddam MJ, Grossar H (2023) Advancements, deficiencies, and future necessities of studying Saprolegniales: A semi-quantitative review of 1073 published Papers. Fungal Biol Rev 46:100319. https://doi.org/10.1016/j.fbr.2023.100319

    Article  CAS  Google Scholar 

  • Milanez AI (1989) Fungos de águas continentais. In: Fidalgo O, Bononi VL, coords. Técnicas de coleta, preservação e herborização de material botânico. São Paulo, Brazil: Série documentos, pp 17–20

  • Milanez AI, Pires-Zottarelli CLA, Gomes AL (2007) Brazilian Zoosporic Fungi. São Paulo, Brasil, 1–113

  • Miranda ML, Pires-Zottarelli CLA (2012) Oomicetos do Parque Estadual da Serra da Cantareira, São Paulo, SP, Brasil. Hoehnea 39:95–112. https://doi.org/10.1590/S2236-89062012000100005

    Article  Google Scholar 

  • Mishra B, Ploch S, Weiland C, Thines M (2023) The TrEase web service: inferring phylogenetic trees with ease. Mycol Prog 22(84):1–6. https://doi.org/10.1007/s11557-023-01931-3

    Article  Google Scholar 

  • Osman A, Ali B, Hashem M, Mostafa M, Mekkawy I (2010) Genotoxicity of two pathogenic strains of zoosporic fungi (Achlya klebsiana and Aphanomyces laevis) on erythrocytes of Nile tilapia Oreochromis niloticus niloticus. Ecotoxicol Environ Saf 73:24–31. https://doi.org/10.1016/j.ecoenv.2009.08.021

    Article  CAS  PubMed  Google Scholar 

  • Pires-Zottarelli CLA, Rocha M (2007) Novas citações de Chytridiomycota e Oomycota para o Parque Estadual das Fontes do Ipiranga (PEFI), SP, Brasil. Acta Bot Bras 21:125–136. https://doi.org/10.1590/S0102-33062007000100012

    Article  Google Scholar 

  • Pires-Zottarelli CLA, Colombo DRS, da Paixão SCO, Ventura PO, Boro MC, Jesus AL (2019) Aphanomyces brasiliensis sp. nov. (Verrucalvaceae, Saprolegniales): a new species from Brazilian Atlantic Rainforest areas. Phytotaxa 415:208–216. https://doi.org/10.11646/phytotaxa.415.4.5

  • Pires-Zottarelli CLA, da Paixão SCO, Colombo DRS, Boro MC, Jesus AL (2022) Saprolegnia atlantica sp. nov. (Oomycota, Saprolegniaceae) from Brazil, and new synonymizations and epitypifications in the genus Saprolegnia. Mycol Prog 21:41. https://doi.org/10.1007/s11557-022-01784-2

  • Pires-Zottarelli CLA, Jesus AL, Colombo DRS, Ventura PO, Boro MC (2023) Occurrence and distribution of the heterotrophic straminipiles from Brazilian Atlantic Rainforest areas. Hoehnea. In SciELO Preprints. https://doi.org/10.1590/2236-8906-39/2022

  • Pires-Zottarelli CLA, Milanez AI, Schoenlein-Crusius IH, Lohmann LG (1996) Criptógamos do Parque Estadual das Fontes do Ipiranga, São Paulo, SP. Fungos, 4: Saprolegniales. Hoehnea 23:39–66

  • Price MN, Dehal PS, Arkin AP (2010) FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS ONE 5(3):e9490. https://doi.org/10.1371/journal.pone.0009490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riethmüller A, Voglmayr H, Göker 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. https://doi.org/10.2307/3761698

    Article  PubMed  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. https://doi.org/10.1139/b99-163

    Article  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. https://doi.org/10.1111/j.1755-0998.2011.03041.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rocha SCO, Jerônimo GH, Marano AV, de Souza JI, Jesus AL, Pires-Zottarelli CLA (2016a) Oomycota from “Parque Estadual da Ilha do Cardoso” (PEIC): first records for São Paulo State and Brazil. Cryptogamie, Mycol 37:177–191. https://doi.org/10.7872/crym/v37.iss2.2016.177

    Article  Google Scholar 

  • Rocha SCO, Lopez-Lastra CC, Marano AV, de Souza JI, Ruéda-Paramo ME, Pires-Zottarelli CLA (2018) New phylogenetic insights into Saprolegniales (Oomycota, Straminipila) based upon studies of specimens from Brazil and Argentina. Mycol Prog 17:691–700. https://doi.org/10.1007/s11557-018-1381-x

    Article  Google Scholar 

  • Rocha SCO, Sandoval-Sierra JV, Diéguez-Uribeondo J, Gonçalves DR, Jerônimo GH, Jesus AL, Marano AV, Pires-Zottarelli CLA (2016b) Saprolegnia milanezii sp. nov., a new species of Saprolegniales (Oomycota, Straminipila) from Brazil. Phytotaxa 270:286–294. https://doi.org/10.11646/phytotaxa.270.4.5

  • Rogers AL, Milanez AI, Beneke ES (1970) Additional aquatic fungi from São Paulo State. Rickia 5:93–110

    Google Scholar 

  • Sandoval-Sierra JV, Diégues-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:e01329999

  • Sandoval-Sierra JV, Martín MP, Diéguez-Uribeondo J (2014) Species identification in the genus Saprolegnia (Oomycetes): defining DNA-based molecular operational taxonomic units. Fungal Biol 118:559–578. https://doi.org/10.1016/j.funbio.2013.10.005

    Article  CAS  PubMed  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

    Chapter  Google Scholar 

  • Schmitz A, Riesner D (2006) Purification of nucleic acids by selective precipitation with polyethylene glycol 6000. Anal Biochem 354:311–313. https://doi.org/10.1016/j.ab.2006.03.014

    Article  CAS  PubMed  Google Scholar 

  • Schoenlein-Crusius IH, Milanez AI (1998) Fungos zoospóricos (Mastigomycotina) da Mata Atlântica da Reserva Biológica do Alto da Serra de Paranapiacaba, município de Santo André, SP. Rev Bras Bot 2:177–181. https://doi.org/10.1590/S0100-84041998000200010

    Article  Google Scholar 

  • Schoenlein-Crusius IH, Milanez AI, Trufem SFB, Pires-Zottarelli CLA, Grandi RAP, Santos ML, Giustra KC (2006) Microscopic fungi in the Atlantic rainforest in Cubatão, São Paulo, Brazil. Braz J Microbiol 37:244–252. https://doi.org/10.1590/S1517-83822006000300014

    Article  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. https://doi.org/10.1017/S0953756202005889

    Article  CAS  Google Scholar 

  • Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steciow MM, Lara H, Pillonel A, Pelizza SA, Lestani EA, Rossi GC, Belhari L (2013) Incipient loss of flagella in the genus Geolegnia: the emergence of a new clade with Leptolegnia? IMA Fungus 4:169–175. https://doi.org/10.5598/imafungus.2013.04.02.02

    Article  PubMed  PubMed Central  Google Scholar 

  • Steciow MM, Lara E, Paul C, Pillonel A, Belhari 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. https://doi.org/10.5598/imafungus.2014.05.02.08

    Article  PubMed  PubMed Central  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 America. Darwiniana 50:25–32. http://www.scielo.org.ar/scielo.php?script=sci_arttext&pid=S0011-67932012000100002

  • Turland NJ, Wiersema JH, Barrie FR, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Kusber W-H, Li D-Z, Marhold K, May TW, McNeill J, Monro AM, Prado J, Price MJ, Smith GF (eds) (2018) International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Glashütten: Koeltz Botanical Books. https://doi.org/10.12705/Code.2018

  • Webster RK, Hall DH, Heeres J, Wick CM, Brandon DM (1970) Achlya klebsiana and Pythium species as primary causes of seed rot and seedling disease of rice in California. Phytopathology 60:964–3968. https://doi.org/10.1094/Phyto-60-964

    Article  Google Scholar 

  • Willoughby LG (2003) Diseases of freshwater fishes. In: Tsui CKM, Hyde KD (eds) Freshwater Mycology. Fungal Diversity Press, China, pp, 111–126

  • Wu Q, Thiers BM, Pfister DH (2004) Preparation, preservation and use of fungal specimens in herbaria. In: Muller GM, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring methods. Elsevier Academic Press, San Diego, pp 23–36. https://doi.org/10.1016/b978-012509551-8/50005-2

Download references

Acknowledgements

We thank “Instituto Florestal” for permission to collect samples in the studied areas and Otto Hartung and Manoel Osorio Neves Junior for their help during sampling. We also thank Poliana de Oliveira Ventura and Ms. Débora Rodrigues da Silva Colombo for their technical help.

Funding

We wish to thank “Fundação de Amparo à Pesquisa do Estado de São Paulo” (FAPESP) for the financial support given to Carmen Lidia Amorim Pires-Zottarelli (Process nº. 2012/50222–7 and 2016/11146-4) and Sarah Cristina de Oliveira da Paixão (Process nº 2016/18787–5). “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) is also acknowledged for the grant given to Carmen Lidia Amorim Pires-Zottarelli (Process CNPq nº 304091/2018–9) and Sarah Cristina de Oliveira da Paixão (Process CNPq nº 152741/2016) and “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES) for the financial support given to Sarah Cristina de Oliveira da Paixão through her post-graduation program. Marco Thines is funded by the excellence initiative of the government of Hesse in the framework of the LOEWE Centre for Translational Biodiversity Genomics (TBG).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carmen Lidia Amorim Pires-Zottarelli.

Ethics declarations

Financial interests

The authors declare they have no financial interests.

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethics approval

Not applicable.

Consent to participate and consent for publication

All authors have contributed to this work. They have also read and commented on the manuscript and accepted its publication in Mycological Progress. This manuscript represents original work that is not being considered for publication, in whole or in part, in another journal, book, conference proceedings, or government publication with a substantial circulation.

Additional information

Section Editor: Tanay Bose

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pires-Zottarelli, C.L.A., de Oliveira da Paixão, S.C., Marano, A.V. et al. Morphological and phylogenetic analyses of Saprolegniales (Oomycota) reveal taxonomic and nomenclatural novelties. Mycol Progress 23, 24 (2024). https://doi.org/10.1007/s11557-024-01963-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11557-024-01963-3

Keywords

Navigation