During an oomycete survey in December 2015, 10 previously unknown Halophytophthora taxa were isolated from marine and brackish water of tidal ponds and channels in saltmarshes, lagoon ecosystems and river estuaries at seven sites along the Algarve coast in the South of Portugal. Phylogenetic analyses of LSU and ITS datasets, comprising all described Halophytophthora species, the 10 new Halophytophthora taxa and all relevant and distinctive sequences available from GenBank, provided an updated phylogeny of the genus Halophytophthora s.str. showing for the first time a structure of 10 clades designated as Clades 1-10. Nine of the 10 new Halophytophthora taxa resided in Clade 6 together with H. polymorphica and H. vesicula. Based on differences in morphology and temperature-growth relations and a multigene (LSU, ITS, Btub, hsp90, rpl10, tigA, cox1, nadh1, rps10) phylo-geny, eight new Halophytophthora taxa from Portugal are described here as H. brevisporangia, H. cele-ris, H. frigida, H. lateralis, H. lusitanica, H. macrosporangia, H. sinuata and H. thermoambigua. Three species, H. frigida, H. macrosporangia and H. sinuata, have a homothallic breeding system while the remaining five species are sterile. Pathogenicity and litter decomposition tests are underway to clarify their pathological and ecological role in the marine and brackish-water ecosystems. More oomycete surveys in yet undersurveyed regions of the world and population genetic or phylogenomic analyses of global populations are needed to clarify the origin of the new Halophytophthora species. Citation: Maia C, Horta Jung M, Carella G, et al. 2022. Eight new Halophytophthora species from marine and brackish-water ecosystems in Portugal and an updated phylogeny for the genus. Persoonia 48: 54 - 90. https://doi.org/10.3767/persoonia.2022.48.02..

Centre of Marine Sciences University of Algarve 8005 139 Faro Portugal

Dipartimento di Agraria Università Mediterranea di Reggio Calabria 89122 Reggio Calabria Italy

Mediterranean Institute for Agriculture Environment and Development University of Algarve 8005 139 Faro Portugal

Mendel University in Brno Faculty of Forestry and Wood Technology Department of Forest Protection and Wildlife Management Phytophthora Research Centre 613 00 Brno Czech Republic

University of Florence Department of Agri Food Production and Environmental Sciences Plant Pathology and Entomology Division 50144 Florence Italy

See more in PubMed

Anastasiou CJ, Churchland LM. 1969. Fungi on decaying leaves in marine habitats. Canadian Journal of Botany 47: 251–257.

Aram K, Rizzo DM.2019. Phytophthora ramorum and Phytophthora gona­podyides differently colonize and contribute to the decomposition of green and senesced Umbellularia californica leaves in a simulated stream environment. Forests 10: 434.

Badis Y, Klochkova TA, Strittmatter M. et al. 2019. Novel species of the oomycete Olpidiopsis potentially threaten European red algal cultivation. Journal of Applied Phycology 31: 1239–1250.

Bennett RM, Cock AWAM, Lévesque A. et al. 2017a. Calycofera gen. nov., an estuarine sister taxon to Phytopythium, Peronosporaceae. Mycological Progress 16: 947–954.

Bennett RM, Devanadera MK, Dedeles GR. et al. 2018. A revision of Salis­pina, its placement in a new family, Salispinaceae (Rhipidiales), and de-scription of a fourth species, S. hoi sp. nov. IMA Fungus 9: 259–269. PubMed PMC

Bennett RM, Nam B, Dedeles GR. et al. 2017b. Phytopythium leanoi sp. nov. and Phytopythium dogmae sp. nov., Phytopythium species associated with mangrove leaf litter from the Philippines. Acta Mycologia 52: 1103.

Bennett RM. Thines M. 2019. Revisiting Salisapiliaceae. Fungal Systematics and Evolution 3: 171–184. PubMed PMC

Bennett RM, Thines M. 2020. An overview on Philippine estuarine oomycetes. Philippine Journal of Systematic Biology 14: 1–14.

Blair JE, Coffey MD, Park S-Y. et al. 2008. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 45: 266–277. PubMed

Botella L, Janoušek J, Maia C. et al. 2020. Marine oomycetes of the genus Halophytophthora harbor viruses related to Bunyaviruses. Frontiers in Microbiology 11: 1467. PubMed PMC

Botella L, Jung T. 2021. Multiple viral infections detected in Phytophthora condilina by total and small RNA sequencing. Viruses 13: 620. PubMed PMC

Brakel J, Werner FJ, Tams V. et al. 2014. Current European Labyrinthula zosterae are not virulent and modulate seagrass (Zostera marina) defense gene expression. PLoS One 9: e92448. PubMed PMC

Brasier CM, Cooke DEL, Duncan JM. et al. 2003. Multiple new phenotypic taxa from trees and riparian ecosystems in Phytophthora gonapodyides – P. megasperma ITS Clade 6, which tend to be high-temperature tolerant and either inbreeding or sterile. Mycological Research 107: 277–290. PubMed

Buaya AT, Ploch S, Inaba S. et al. 2019. Holocarpic oomycetes parasitoids of red algae are not Olpidiopsis. Fungal Systematics and Evolution 4: 21–31. PubMed PMC

Buaya AT, Scholz B, Thines M. 2021. Sirolpidium bryopsidis, a parasite of green algae, is probably conspecific with Pontisma lagenidioides, a parasite of red algae. Fungal Systematics and Evolution 7: 223–231. PubMed PMC

Caballol M, Štraus D, Macia H. et al. 2021. Halophytophthora fluviatilis pathogenicity and distribution along a Mediterranean-subalpine gradient. Journal of Fungi 7: 112. PubMed PMC

Cooke DEL, Drenth A, Duncan JM. et al. 2000. A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genetics and Biology 30: 17–32. PubMed

De Cock AWAM, Lodhi AM, Rintoul TL. et al. 2015. Phytopythium: molecular phylogeny and systematics. Persoonia 34: 25–39. PubMed PMC

Dick MW. 1990. Keys to Pythium. University of Reading Press, Reading, UK.

Drake LA, Doblin MA, Dobbs FC. 2007. Potential microbial bioinvasions via ships’ ballast water, sediment, and biofilm. Marine Pollution Bulletin 55: 333–341. PubMed

Edler D, Klein J, Antonelli A. et al. 2021. raxmlGUI 2.0: A graphical interface and toolkit for phylogenetic analyses using RAxML. Methods in Ecology and Evolution 12: 373–377.

Erwin DC, Ribeiro OK. 1996. Phytophthora diseases worldwide. APS Press St. Paul, Minnesota.

Fell JW, Master IM. 1975. Phycomycetes (Phytophthora spp. nov. and Pythium sp. nov.) associated with mangrove (Rhizophora mangle) leaves. Canadian Journal of Botany 53: 2908–2922.

Foster ZSL, Albornoz FE, Fieland VJ. et al. 2021. A new oomycete metabarcoding method using the rps10 gene. bioRxiv: 2021.09.22.460084

Gachon CMM, Strittmatter M, Badis Y. et al. 2017. Pathogens of brown algae: culture studies of Anisolpidium ectocarpii and A. rosenvingei reveal that the Anisolpidiales are uniflagellated oomycetes. European Journal of Phycology 52: 133–148.

Gachon CMM, Strittmatter M, Müller DG. et al. 2009. Detection of differential host susceptibility to the marine oomycete pathogen Eurychasma dicksonii by real-time PCR: not all algae are equal. Applied and Environmental Microbiology 75: 322–328. PubMed PMC

Garbelotto MM, Lee HK, Slaughter G. et al. 1997. Heterokaryosis is not required for virulence of Heterobasidion annosum. Mycologia 89: 92–102.

Garvetto A, Perrineau M-M, Dressler-Allame M. et al. 2020. ‘Ectrogella’ parasitoids of the diatom Licmophora sp. are polyphyletic. Journal of Eukaryotic Microbiology 67: 18–27. PubMed

Gerrettson-Cornell L, Simpson J. 1984. Three new marine Phytophthora species from New South Wales. Mycotaxon 19: 453–470.

Govers LL, Man in ´t Veld WA, Meffert JP. et al. 2016. Marine Phytophthora species can hamper conservation and restoration of vegetated coastal ecosystems. Proceedings of the Royal Society B: Biological Sciences 283: 20160812. PubMed PMC

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

Ho HH, Chang HS, Huang SH. 2003. Halophytophthora elongata, a new marine species from Taiwan. Mycotaxon 85: 417–422.

Ho HH, Jong SC. 1990. Halophytophthora, gen nov., a new member of the family Pythiaceae. Mycotaxon 36: 377–382.

Ho HH, Nakagiri A, Newell SY. 1992. A new species of Halophytophthora from Atlantic and Pacific subtropical islands. Mycologia 84: 548–554.

Hopple JS, Vilgalys R. 1994. Phylogenetic relationships among coprinoid taxa and allies based on data from restriction site mapping of nuclear rDNA. Mycologia 86: 96–107.

Hüberli D, Hardy GEStJ, White D. et al. 2013. Fishing for Phytophthora from Western Australia’s waterways: A distribution and diversity survey. Australasian Plant Pathology 42: 251–260.

Hulvey J, Telle S, Nigrelli L. et al. 2010. Salisapiliaceae – a new family of oomycetes from marsh grass litter of southeastern North America. Persoonia 25: 109–116. PubMed PMC

Jesus AL, Marano AV, Gonçalve DR. et al. 2019. Two new species of Halophytophthora from Brazil. Mycological Progress 18: 1411–1421.

Jesus AL, Marano AV, Jerônimo GH. et al. 2016. The genus Halophytophthora (Peronosporales, Straminipila) in Brazil: first descriptions of species. Brazilian Journal of Botany 39: 729–739.

Jung T, Blaschke H, Neumann P. 1996. Isolation, identification and pathogenicity of Phytophthora species from declining oak stands. European Journal of Forest Pathology 26: 253–272.

Jung T, Burgess TI.. 2009. Re-evaluation of Phytophthora citricola isolates from multiple woody hosts in Europe and North America reveals a new species Phytophthora plurivora sp nov. Persoonia 22: 95–110. PubMed PMC

Jung T, Chang TT, Bakonyi J. et al. 2017a. Diversity of Phytophthora species in natural ecosystems of Taiwan and association with disease symptoms. Plant Pathology 66: 194–211.

Jung T, Cooke DEL, Blaschke H. et al. 1999. Phytophthora quercina sp. nov., causing root rot of European oaks. . Mycological Research 103: 785–798.

Jung T, Horta Jung M, Cacciola SO. et al. 2017b. Multiple new cryptic pathogenic Phytophthora species from Fagaceae forests in Austria, Italy and Portugal. IMA Fungus 8: 219–244. PubMed PMC

Jung T, Horta Jung M, Scanu B. et al. 2017c. Six new Phytophthora species from ITS Clade 7a including two sexually functional heterothallic hybrid species detected in natural ecosystems in Taiwan. Persoonia 38: 100–135. PubMed PMC

Jung T, Horta Jung M, Webber JF.et al. 2021. The destructive tree pathogen Phytophthora ramorum originates from the Laurosilva forests of East Asia. Journal of Fungi 7: 226. PubMed PMC

Jung T, Pérez-Sierra A, Durán A. et al. 2018. Canker and decline diseases caused by soil- and airborne Phytophthora species in forests and woodlands. Persoonia 40: 182–220. PubMed PMC

Jung T, Scanu B, Bakonyi J. et al. 2017d. Nothophytophthora gen. nov., a new sister genus of Phytophthora from natural and semi-natural ecosystems. Persoonia 39: 143–174. PubMed PMC

Jung T, Stukely MJC, Hardy GEStJ. et al. 2011. Multiple new Phytophthora species from ITS Clade 6 associated with natural ecosystems in Australia: evolutionary and ecological implications. Persoonia 26: 13–39. PubMed PMC

Katoh K, Standley DM. 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution 30: 772–780. PubMed PMC

Kroon LPNM, Bakker FT, Van den Bosch GBM, et al. 2004. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genetics and Biology 41: 766–782. PubMed

Kumar S, Stecher G, Li M. et al. 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35: 1547–1549. PubMed PMC

Lamour K. (ed). 2013. Phytophthora: A global perspective. CABI, Wallingford, UK.

Lamour KH, Finley L. 2006. A strategy for recovering high quality genomic DNA from a large number of Phytophthora isolates. Mycologia 98: 514–517. PubMed

Lara E, Belbahri L. 2011. SSU rRNA reveals major trends in oomycete evolution. Fungal Diversity 49: 93–100.

Leaño EM, Jones EBG, Vrijmoed LLP. 2000. Why are Halophytophthora species well adapted to mangrove habitats? In: Hyde KD, Ho WH, Pointing SB. (eds), Aquatic mycology across the Fungal Diversity 5: 131–151.

Leaño EM, Vrijmoed LLP, Jones ERG. 1998. Physiological studies on Halophytophthora vesicula (straminipilous fungi) isolated from fallen mangrove leaves from Mai Po, Hong Kong. Botanica Marina 41: 411–419.

Li GJ, Hyde KD, Zhao RL.et al. 2016. Fungal diversity notes 253–366: taxonomic and phylogenetic contributions to fungal taxa. Fungal Diversity 78: 1–237.

Man in ‘t Veld WA, Rosendahl KC, Brouwer H, et al. 2011. Phytophthora gemini sp. nov., a new species isolated from the halophilic plant Zostera marina in the Netherlands. Fungal Biology 115: 724–732. PubMed

Man in ‘t Veld WA, Rosendahl KCHM, Van Rijswick PCJ. et al. 2019. Multiple Halophytophthora spp. and Phytophthora spp. including P. gemini, P. inundata and P. chesapeakensis sp. nov.isolated from the seagrass Zostera marina in the Northern hemisphere. European Journal of Plant Pathology 153: 341–357.

Marano AV, Jesus AL, De Souza JI. et al. 2016. Ecological roles of saprotrophic Peronosporales (Oomycetes, Straminipila) in natural environments. Fungal Ecology 19: 77–88.

Martin DL, Chiari Y, Boone E. et al. 2016. Functional, phylogenetic and host-geographic signatures of Labyrinthula spp. provide for putative species delimitation and a global-scale view of seagrass wasting disease. Estuaries and Coasts 39: 1403–1421.

Martin FN, Tooley PW. 2003. Phylogenetic relationships among Phytophthora species inferred from sequence analysis of mitochondrially encoded cytochrome oxidase I and II genes. Mycologia 95: 269–284. PubMed

Muehlstein LK, Porter D, Short FT. 1988. Labyrinthula sp., a marine slime mold producing symptoms of wasting disease in eelgrass, Zostera marina. Marine Biology 99: 465–472.

Nakagiri A. 2000. Ecology and biodiversity of Halophytophthora species. In: Hyde KD, Ho WH, Pointing SB. (eds), Aquatic mycology across the Millennium. Fungal Diversity 5: 153–164.

Nakagiri A, Ito T, Manoch L. et al. 2001. A new Halophytophthora species, H. porrigovesica, from subtropical and tropical mangroves. Mycoscience 42: 33–41.

Nakagiri A, Newell SY, Ito T. 1994. Two new Halophytophthora species, H. tar-tarea and H. masteri, from intertidal decomposing leaves in saltmarsh and mangrove regions. Mycoscience 35: 223–232.

Newell SY, Fell JW. 1992. Distribution and experimental responses to sub­strate of marine oomycetes (Halophytophthora spp.) in mangrove ecosystems. Mycological Research 96: 851–856.

Newell SY, Fell JW. 1995. Do halophytophthoras (marine Pythiaceae) rapidly occupy fallen leaves by intraleaf mycelial growth? Canadian Journal of Botany 73:761–765.

Newell SY, Miller JD, Fell JW. 1987. Rapid and pervasive occupation of fallen mangrove leaves by a marine zoosporic fungus. Applied and Environmental Microbiology 53: 2464–2469. PubMed PMC

Nigrelli L, Thines M. 2013. Tropical oomycetes in the German Bight – Climate warming or overlooked diversity? Fungal Ecology 6: 152–160.

Pegg KG, Alcorn JL. 1982. Phytophthora operculata sp. nov. a new marine fungus. Mycotaxon 16: 99–102.

Pegg KG, Gillespie NC, Forsberg LI. 1980. Phytophthora sp. associated with mangrove death in Central Coastal Queensland. Australasian Plant Pathology 9: 6–7.

Raghukumar S, Sathe-Pathak V, Sharma S, et al. 1995. Thraustochytrid and fungal component of marine detritus 111. Field studies on decomposition of leaves of the mangrove Rhizophora apiculata. Aquatic Microbial Ecology 9: 117–125.

Rahman MZ, Uematsu S, Coffey MD. et al. 2014. Re-evaluation of Japanese Phytophthora isolates based on molecular phylogenetic analyses. Mycoscience 55: 314–327.

Reeser PW, Sutton W, Hansen EM. et al. 2011. Phytophthora species in forest streams in Oregon and Alaska. Mycologia 103: 22–35. PubMed

Robideau GP, De Cock AW, Coffey MD. et al. 2011. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Molecular Ecology Resources 11: 1002–1011 PubMed PMC

Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574. PubMed

Ruiz GM, Fofonoff PW, Carlton JT. et al. 2000b. Invasion of coastal marine communities in North America: Apparent patterns, processes, and biases. Annual Review of Ecology and Systematics 31: 481–531.

Ruiz GM, Rawlings TK, Dobbs FC. et al. 2000a. Global spread of micro­organisms by ships. Nature 408: 49–50. PubMed

Santschi F, Gounand I, Harvey E. et al. 2017. Leaf litter diversity and structure of microbial decomposer communities modulate litter decomposition in aquatic systems. Functional Ecology 32: 522–532.

Shakya SK, Grünwald NJ, Fieland VJ. et al. 2021. Phylogeography of the wide-host range panglobal plant pathogen Phytophthora cinnamomi. Molecular Ecology 30: 5164–5178. PubMed

Sparrow FK. 1960. Aquatic Phycomycetes. The University of Michigan Press, Ann Arbor, USA.

Stöver BC, Müller KF. 2010. TreeGraph 2: Combining and visualizing evi­dence from different phylogenetic analyses. BMC Bioinformatics 11: 7. PubMed PMC

Su CJ, Hsieh SY, Chiang MWL. et al. 2020. Salinity, pH and temperature growth ranges of Halophytophthora isolates suggest their physiological adaptations to mangrove environments. Mycology 11: 256–262. PubMed PMC

Sullivan BK, Trevathan-Tackett SM, Neuhauser S. et al. 2018. Host-pathogen dynamics of seagrass diseases under future global change. Marine Pollution Bulletin 134: 75–88. PubMed PMC

Tan TK, Pek CL. 1997. Tropical mangrove leaf litter fungi in Singapore with an emphasis on Halophytophthora. Mycological Research 101: 165–168.

Thines M. 2014. Phylogeny and evolution of plant pathogenic oomycetes – a global overview. European Journal of Plant Pathology 38: 431–447.

Vergeer LHT, Den Hartog C. 1994. Omnipresence of Labyrinthulaceae in seagrasses. Aquatic Botany 48: 1–20.

West JA, Klochkova TA, Kim GH. et al. 2006. Olpidiopsis sp., an oomycete from Madagascar that infects Bostrychia and other red algae: Host species susceptibility. Phycological Research 54: 72–85.

White TJ, Bruns T, Lee S. et al. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Gelfand DH, Sninsky JJ, Innes MA, et al. (eds), PCR protocols: a guide to methods and applications: 315– 322. Academic Press, San Diego, California, USA.

Yang X, Hong C. 2014. Halophytophthora fluviatilis sp.nov. from freshwater in Virginia. FEMS Microbiology Letters 352: 230–237. PubMed

Phytophthora, Nothophytophthora and Halophytophthora diversity in rivers, streams and riparian alder ecosystems of Central Europe

Synchrospora gen. nov., a New Peronosporaceae Genus with Aerial Lifestyle from a Natural Cloud Forest in Panama

Unravelling the Lipids Content and the Fatty Acid Profiles of Eight Recently Described Halophytophthora Species and H. avicennae from the South Coast of Portugal

Phytophthora: an ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation

High Diversity of Novel Viruses in the Tree Pathogen Phytophthora castaneae Revealed by High-Throughput Sequencing of Total and Small RNA

See more in PubMed

Dryad
10.5061/dryad.gf1vhhmr2