Marine oomycetes

Marine oomycetes are species of oomycete that inhabit oceans, coastal, and estuarine environments.[1] They belong to the phylum oomycota and kingdom stramenopila, occupying diverse roles as parasites, pathogen and saprophytes infecting diatoms, algae, plants, and animals, or consuming dead organic matter in water.[2][3][4] These organisms contribute significantly to nutrient cycling, and host population dynamics in marine ecological niches.[5]

Characteristics

Marine oomycetes are heterotrophic, filamentous eukaryotic organisms that have morphological features similar to fungi, characterized by mycelial growth, modes of reproduction and infection.[6][2] Historically, these similarities led them to be classified as fungi. However, later morphological, molecular and phylogenetic analyses placed them within the Kingdom Stramenopile, making them more closely related to algae, diatoms, and plants.[7]

The cell walls of marine oomycetes are primarily composed of β-1,3- and β-1,6-glucans, along with cellulose, a composition that distinguishes them from true fungi, which typically have chitin-rich cell walls.[8] Their vegetative hyphae are generally hyaline (transparent) and often lack septation.[9]

Marine oomycetes exhibit diverse roles in nature like decomposing organic matter such as leaf debris in coastal marine environments while many infecting a range of hosts including marine algae, diatoms, vertebrates and invertebrates.[1][6][10][11]

Life and reproduction

Marine oomycetes reproduction involves the formation of asexual reproductive fruiting bodies called sporangia on specialized hyphae.[9] These sporangia release motile zoospores, which exhibit directional swimming behavior to locate suitable hosts for infection.[10][12] Zoospores are asexual biflagellate spores without a cell wall that can swim in water acting as propagules of infections.[9][13] They navigate their environment by responding to various stimuli, including chemical gradients (chemotaxis), and electrical fields (electrotaxis).[13][1] This targeted movement helps zoospores to find and infect hosts in marine environments.

Once a zoospore lands on a suitable host surface like a marine diatom, it sticks to it, sheds off or retracts its flagella, and develops a cell wall in a process called encystment.[13][11] Upon successful penetrating into the host by developing specialized hyphae, a special structure called thallus emerges to feed on nutrients of host and further reproduce.[11][14] Most of the marine oomycetes infecting diatoms, algae and invertebrates are holocarpic i.e. the entire thallus can transform into a sporangium, releasing new zoospores to continue the cycle.[15][16][6] However, not all marine oomycetes are holocarpic, and some are eucarpic.[17][18] In these species only a portion of the thallus becomes reproductive while the rest remains vegetative.

Sexual reproduction in marine oomycetes involves production of resting sexual oospores.[16] While it has been reported to occur in the genus Olpidiopsis, there is a limited information in marine oomycetes overall.[19]

Role in infection

Microorganisms

Marine oomycetes are important intracellular parasitoids of microorganisms, particularly diatoms, in coastal and open-ocean ecosystems. Marine oomycetes parasitizing diatoms have been detected in the Arctic Ocean, Northwest Iceland, North Atlantic coastal waters, and the pacific northwestern coast of United States.[5][15][11][20] These include species of Ectrogella, Lagenisma, Olpidiopsis, and Miracula, infecting different diatoms such as Licmophora, Pseudo-nitzschia, Coscinodiscus, and[21] Minidiscus.[11][22][14][15][5][20] Some marine oomycetes also target toxin-producing diatoms, notably species of Pseudo-nitzschia.[11][22] A study has shown that a marine oomycete species can rewire the metabolome of its host diatom to control host physiology and promote infection.[14]

Plants and seaweeds

Marine oomycetes also infect various plant and algal species, particularly in coastal and estuarine environments. Species of Halophytophthora, colonize fallen leaves of the red mangrove tree in tropical and subtropical regions.[3] These oomycetes act primarily as saprotrophs, decomposing fallen plant material, but some species can also be pathogenic to living hosts. Halophytophthora zosterae has been reported to restrict seed viability and seedling development of the eelgrass zostera marina along the coast of North america and Eurasia.[1] Another species, Pythium marinum is a facultative parasite of the red alga Porphyra miniata.[23]

Animals

Some marine holocarpic pathogens can infect animals such as nematodes, crustaceans, and mollusks.[2][16] Lagenidium callinectes infects the eggs of the blue crab, while Halioticida noduliformans has been reported to infect the eggs of european lobster.[24][25] Pythium flevoense was identified as the cause of dermatitis in the harbor porpoise, marking one of the first cases of a marine mammal infected by an oomycete.[4] In addition, this pathogen can also infect freshwater copepods and ayu fish larvae.[26][27]

Role in ecology

Marine oomycetes play a crucial role in shaping coastal and open-ocean ecosystems as decomposers of sea litter and parasites of planktons, particularly diatoms. Several species including from genera Lagenisma can potentially regulate algal blooms by parasitizing phytoplankton like species of Coscinodiscus and Cerataulina during periods of high abundance, although the extent of their influence remains uncertain.[14][11][6] In mangrove ecosystems, species of Halophytophthora act as major saprophytic decomposers of fallen mangrove leaves, playing a vital part in nutrient cycling.[3] In Arctic environments, some marine oomycetes have been reported to encode genes involved in carbon cycling such as those for carbohydrate metabolism (e.g. pectate lyase, chitinase, mannanase), possibly playing roles in both microbial food webs and biogeochemical cycling of carbon.[5] The ongoing warming of oceans due to climate change may increase their ecological impact by introducing lower-latitude species into new regions, potentially reshaping primary producer communities.[5]

References

  1. 1 2 3 4 Botella, Leticia; Janoušek, Josef; Maia, Cristiana; Jung, Marilia Horta; Raco, Milica; Jung, Thomas (2020-07-15). "Marine Oomycetes of the Genus Halophytophthora Harbor Viruses Related to Bunyaviruses". Frontiers in Microbiology. 11: 1467. doi:10.3389/fmicb.2020.01467. ISSN 1664-302X. PMC 7375090. PMID 32760358.
  2. 1 2 3 Beakes, Gordon W.; Glockling, Sally L.; Sekimoto, Satoshi (January 2012). "The evolutionary phylogeny of the oomycete "fungi"". Protoplasma. 249 (1): 3–19. Bibcode:2012Prpls.249....3B. doi:10.1007/s00709-011-0269-2. ISSN 0033-183X. PMID 21424613.
  3. 1 2 3 Newell, S.Y.; Fell, J.W. (October 1992). "Distribution and experimental responses to substrate of marine oomycetes (Halophytophthora spp.) in mangrove ecosystems". Mycological Research. 96 (10): 851–856. doi:10.1016/S0953-7562(09)81030-7.
  4. 1 2 Veldhuis Kroeze, Edwin J. B.; van Elk, Cornelis E.; van de Bildt, Marco W. G.; van Run, Peter R. W. A.; Foster, Geoffrey; Abou-Chakra, Nissrine; Hare, Rasmus Krøger; Kuiken, Thijs (2023-11-02). "Infection with Pythium flevoense in a harbour porpoise (Phocoena phocoena) as a novel cause of dermatitis in marine mammals". Veterinary Research. 54 (1): 102. doi:10.1186/s13567-023-01226-1. ISSN 1297-9716. PMC 10623814. PMID 37919808.
  5. 1 2 3 4 5 Hassett, Brandon T.; Thines, Marco; Buaya, Anthony; Ploch, Sebastian; Gradinger, R. (December 2019). "A glimpse into the biogeography, seasonality, and ecological functions of arctic marine Oomycota". IMA Fungus. 10 (1): 6. doi:10.1186/s43008-019-0006-6. ISSN 2210-6359. PMC 7325649. PMID 32647615.
  6. 1 2 3 4 "An overview on the biology and phylogeny of the early-diverging oomycetes" (PDF). Philippine Journal of Systematic Biology. 14 (1). 2020-07-15. doi:10.26757/pjsb2020a14004.
  7. ↑ Rossman, Amy Y.; Palm, Mary E. (2006-10-01). "Why are Phytophthora and Other Oomycota not True Fungi?". Outlooks on Pest Management. 17 (5): 217–219. doi:10.1564/17oct08.
  8. ↑ Mélida, Hugo; Sandoval-Sierra, Jose V.; Diéguez-Uribeondo, Javier; Bulone, Vincent (2013-01-29). "Analyses of Extracellular Carbohydrates in Oomycetes Unveil the Existence of Three Different Cell Wall Types". Eukaryotic Cell. 12 (2): 194–203. doi:10.1128/ec.00288-12. PMC 3571302. PMID 23204192.
  9. 1 2 3 Heffer, V.; Powelson, M. L.; Johnson, K. B. (2002). "Oomycetes". The Plant Health Instructor. doi:10.1094/PHI-I-2002-0225-01. ISSN 1935-9411.
  10. 1 2 Kolátková, Viktorie; Mooney, Megan; Kelly, Kate; Hineva, Elitsa; Gawryluk, Ryan M. R.; Elliott, Joel (August 2023). "Eelgrass ( Zostera spp.) associated phytomyxids are host-specific congeneric parasites and predominant eukaryotes in the eelgrass rhizosphere on a global scale". Environmental Microbiology. 25 (8): 1522–1537. Bibcode:2023EnvMi..25.1522K. doi:10.1111/1462-2920.16376. hdl:1828/16382. ISSN 1462-2912. PMID 36978287.
  11. 1 2 3 4 5 6 7 Garvetto, Andrea; Nézan, Elisabeth; Badis, Yacine; Bilien, Gwenael; Arce, Paola; Bresnan, Eileen; Gachon, Claire M. M.; Siano, Raffaele (2018-12-03). "Novel Widespread Marine Oomycetes Parasitising Diatoms, Including the Toxic Genus Pseudo-nitzschia: Genetic, Morphological, and Ecological Characterisation". Frontiers in Microbiology. 9: 2918. doi:10.3389/fmicb.2018.02918. ISSN 1664-302X. PMC 6286980. PMID 30559730.
  12. ↑ Hatai, Kishio (2012), "Diseases of Fish and Shellfish Caused by Marine Fungi", in Raghukumar, Chandralata (ed.), Biology of Marine Fungi, Progress in Molecular and Subcellular Biology, vol. 53, Berlin, Heidelberg: Springer Berlin Heidelberg, pp. 15–52, doi:10.1007/978-3-642-23342-5_2, ISBN 978-3-642-23341-8, PMID 22222825, retrieved 2025-04-27
  13. 1 2 3 Walker, Claire A.; van West, Pieter (February 2007). "Zoospore development in the oomycetes". Fungal Biology Reviews. 21 (1): 10–18. Bibcode:2007FunBR..21...10W. doi:10.1016/j.fbr.2007.02.001.
  14. 1 2 3 4 Vallet, Marine; Baumeister, Tim U. H.; Kaftan, Filip; Grabe, Veit; Buaya, Anthony; Thines, Marco; Svatoš, Aleš; Pohnert, Georg (2019-10-30). "The oomycete Lagenisma coscinodisci hijacks host alkaloid synthesis during infection of a marine diatom". Nature Communications. 10 (1): 4938. Bibcode:2019NatCo..10.4938V. doi:10.1038/s41467-019-12908-w. ISSN 2041-1723. PMC 6821873. PMID 31666506.{{cite journal}}: CS1 maint: unflagged free DOI (link)
  15. 1 2 3 Buaya, Anthony T.; Scholz, Bettina; Thines, Marco (2021-07-04). "A New Marine Species of Miracula ( Oomycota ) Parasitic to Minidiscus sp. in Icelandtitle". Mycobiology. 49 (4): 355–362. doi:10.1080/12298093.2021.1952813. ISSN 1229-8093. PMC 8409938. PMID 34512079.
  16. 1 2 3 Thines, Marco; Choi, Young-Joon (January 2016). "Evolution, Diversity, and Taxonomy of the Peronosporaceae, with Focus on the Genus Peronospora". Phytopathology. 106 (1): 6–18. Bibcode:2016PhPat.106....6T. doi:10.1094/PHYTO-05-15-0127-RVW. ISSN 0031-949X. PMID 26649784.
  17. ↑ UK, CAB International; Spencer, M. A. (2004-12-31). "Pythium porphyrae. [Descriptions of Fungi and Bacteria]". Descriptions of Fungi and Bacteria: Sheet 1617. doi:10.1079/DFB/20056401617.
  18. ↑ Howard, Kenneth L.; and Johnson Jr., T. W. (1969-05-01). "Aquatic Fungi of Iceland: Some Filamentous, Eucarpic, and Holocarpic Species". Mycologia. 61 (3): 496–510. doi:10.1080/00275514.1969.12018763. ISSN 0027-5514.
  19. ↑ Sekimoto, Satoshi; Yokoo, Kazunari; Kawamura, Yoshio; Honda, Daiske (March 2008). "Taxonomy, molecular phylogeny, and ultrastructural morphology of Olpidiopsis porphyrae sp. nov. (Oomycetes, straminipiles), a unicellular obligate endoparasite of Bangia and Porphyra spp. (Bangiales, Rhodophyta)". Mycological Research. 112 (3): 361–374. doi:10.1016/j.mycres.2007.11.002. PMID 18308530.
  20. 1 2 Sparrow, Frederick K. (1969). "Zoosporic marine fungi from the Pacific Northwest (U.S.A.)". Archiv für Mikrobiologie. 66 (2): 129–146. Bibcode:1969ArMic..66..129S. doi:10.1007/BF00410220. hdl:2027.42/46146. ISSN 0302-8933.
  21. ↑ "Guide to Minidiscus | Genera - Diatoms of North America". diatoms.org. Retrieved 2025-04-29.
  22. 1 2 Hanic, Louis A.; Sekimoto, Satoshi; Bates, Stephen S. (November 2009). "Oomycete and chytrid infections of the marine diatom Pseudo-nitzschia pungens (Bacillariophyceae) from Prince Edward Island, Canada". Botany. 87 (11): 1096–1105. Bibcode:2009Botan..87.1096H. doi:10.1139/B09-070. ISSN 1916-2790.
  23. ↑ Kazama, Frederick Y.; Fuller, Melvin S. (1973-04-01). "Mineral nutrition of Pythium marinum , a marine facultative parasite". Canadian Journal of Botany. 51 (4): 693–699. Bibcode:1973CaJB...51..693K. doi:10.1139/b73-086. ISSN 0008-4026.
  24. ↑ Rogers-Talbert, R. (October 1948). "The Fungus Lagenidium callinectes Couch (1942) on Eggs of the Blue Crab in Chesapeake Bay". The Biological Bulletin. 95 (2): 214–228. doi:10.2307/1538026. ISSN 0006-3185. JSTOR 1538026. PMID 18887846.
  25. ↑ Holt, Corey; Foster, Rachel; Daniels, Carly L.; van der Giezen, Mark; Feist, Stephen W.; Stentiford, Grant D.; Bass, David (May 2018). "Halioticida noduliformans infection in eggs of lobster (Homarus gammarus) reveals its generalist parasitic strategy in marine invertebrates". Journal of Invertebrate Pathology. 154: 109–116. Bibcode:2018JInvP.154..109H. doi:10.1016/j.jip.2018.03.002. PMC 5992330. PMID 29555081.
  26. ↑ Miura, Masayuki; Hatai, Kishio; Tojo, Motoaki; Wada, Shinpei; Kobayashi, Sakura; Okazaki, Takumi (2010). "Visceral Mycosis in Ayu Plecoglossus altivelis Larvae Caused by Pythium flevoense". Fish Pathology. 45 (1): 24–30. doi:10.3147/jsfp.45.24. ISSN 0388-788X.
  27. ↑ Garcia, Rd; Jara, Fg; Steciow, Mm; Reissig, M (2018-07-04). "Oomycete parasites in freshwater copepods of Patagonia: effects on survival and recruitment". Diseases of Aquatic Organisms. 129 (2): 123–134. doi:10.3354/dao03240. hdl:11336/86970. ISSN 0177-5103. PMID 29972373.
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