Skip to main content
SpringerLink
Log in

Enigmatic Phytomyxid Parasite of the Alien Seagrass Halophila stipulacea: New Insights into Its Ecology, Phylogeny, and Distribution in the Mediterranean Sea

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Marine phytomyxids represent often overlooked obligate biotrophic parasites colonizing diatoms, brown algae, and seagrasses. An illustrative example of their enigmatic nature is the phytomyxid infecting the seagrass Halophila stipulacea (a well-known Lessepsian migrant from the Indo-Pacific to the Mediterranean Sea). In the Mediterranean, the occurrence of this phytomyxid was first described in 1995 in the Strait of Messina (southern Italy) and the second time in 2017 in the Aegean coast of Turkey. Here we investigated, using scuba diving, stereomicroscopy, light and scanning electron microscopy, and molecular methods, whether the symbiosis is still present in southern Italy, its distribution in this region and its relation to the previous reports. From the total of 16 localities investigated, the symbiosis has only been found at one site. A seasonal pattern was observed with exceptionally high abundance (> 40% of the leaf petioles colonized) in September 2017, absence of the symbiosis in May/June 2018, and then again high infection rates (~ 30%) in September 2018. In terms of anatomy and morphology as well as resting spore dimensions and arrangement, the symbiosis seems to be identical to the preceding observations in the Mediterranean. According to the phylogenetic analyses of the 18S rRNA gene, the phytomyxid represents the first characterized member of the environmental clade “TAGIRI-5”. Our results provide new clues about its on-site ecology (incl. possible dispersal mechanisms), hint that it is rare but established in the Mediterranean, and encourage further research into its distribution, ecophysiology, and taxonomy.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

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

Similar content being viewed by others

References

  1. Ugarelli K, Chakrabarti S, Laas P, Stingl U (2017) The seagrass holobiont and its microbiome. Microorganisms 5:81

    Article  PubMed Central  CAS  Google Scholar 

  2. Jensen SI, Kühl M, Priemé A (2007) Different bacterial communities associated with the roots and bulk sediment of the seagrass Zostera marina. FEMS Microbiol Ecol 62:108–117

    Article  CAS  PubMed  Google Scholar 

  3. Garcias-Bonet N, Arrieta JM, de Santana CN, Duarte CM, Marbà N (2012) Endophytic bacterial community of a Mediterranean marine angiosperm (Posidonia oceanica). Front Microbiol 3:342

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cúcio C, Engelen AH, Costa R, Muyzer G (2016) Rhizosphere microbiomes of European seagrasses are selected by the plant but are not species specific. Front Microbiol 7:440

    Article  PubMed  PubMed Central  Google Scholar 

  5. Fahimipour AK, Kardish MR, Lang JM, Green JL, Eisen JA, Stachowicz JJ (2017) Global-scale structure of the eelgrass microbiome. Appl Environ Microbiol 83:e03391–e03316

    Article  PubMed  PubMed Central  Google Scholar 

  6. Mata JL, Cebrián J (2013) Fungal endophytes of the seagrasses Halodule wrightii and Thalassia testudinum in the northcentral Gulf of Mexico. Bot Mar 56:541–545

    Article  Google Scholar 

  7. Venkatachalam A, Thirunavukkarasu N, Suryanarayanan TS (2015) Distribution and diversity of endophytes in seagrasses. Fungal Ecol 13:60–65

    Article  Google Scholar 

  8. Vohník M, Borovec O, Kolařík M (2016) Communities of cultivable root mycobionts of the seagrass Posidonia oceanica in the northwest Mediterranean Sea are dominated by a hitherto undescribed pleosporalean dark septate endophyte. Microb Ecol 71:442–451

    Article  PubMed  Google Scholar 

  9. Vohník M, Borovec O, Župan I, Kolařík M, Sudová R (2017) Fungal root symbionts of the seagrass Posidonia oceanica in the central Adriatic Sea revealed by microscopy, culturing and 454-pyrosequencing. Mar Ecol Progr Ser 583:107–120

    Article  CAS  Google Scholar 

  10. Neuhauser S, Kirchmair M, Gleason FH (2011) Ecological roles of the parasitic phytomyxids (plasmodiophorids) in marine ecosystems - a review. Mar Freshwater Res 62:365–371

    Article  CAS  Google Scholar 

  11. Mateu-Vicens G, Khokhlova A, Sebastián-Pastor T (2014) Epiphytic foraminiferal indices as bioindicators in Mediterranean seagrass meadows. J Foram Res 44(3):325–339

    Article  Google Scholar 

  12. Man in’t Veld WA, Rosendahl KC, van Rijswick PC, Meffert JP, Boer E, Westenberg M, van der Heide T, Govers LL (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. Eur J Plant Pathol 153(2):341–357

    Article  Google Scholar 

  13. Muehlstein LK, Porter D, Short FT (1991) Labyrinthula zosterae sp. nov., the causative agent of wasting disease of eelgrass, Zostera marina. Mycologia 83:180–191

    Article  Google Scholar 

  14. Ralph PJ, Short FT (2002) Impact of the wasting disease pathogen, Labyrinthula zosterae, on the photobiology of eelgrass Zostera marina. Mar Ecol Progr Ser 226:265–271

    Article  Google Scholar 

  15. Neuhauser S, Gleason FH, Kirchmair M (2012) Phytomyxea (Super-group Rhizaria). In: Gareth Jones EB, Pang K-L (eds) Marine fungi and fugal-like organisms. De Gruyter, Berlin, pp 245–249

    Chapter  Google Scholar 

  16. Neuhauser S, Kirchmair M, Bulman S, Bass D (2014) Cross-kingdom host shifts of phytomyxid parasites. BMC Evol Biol 14:33

    Article  PubMed  PubMed Central  Google Scholar 

  17. Sullivan BK, Trevathan-Tackett SM, Neuhauser S, Govers LL (2018) Host-pathogen dynamics of seagrass diseases under future global change. Mar Pollut Bull 134:75–88

    Article  CAS  PubMed  Google Scholar 

  18. den Hartog C (1965) Some notes on the distribution of Plasmodiophora diplantherae, a parasitic fungus on species of Halodule. Persoonia 4:15–18

    Google Scholar 

  19. den Hartog C (1989) Distribution of Plasmodiophora bicaudata, a parasitic fungus on small Zostera species. Dis Aquat Organ 6:227–229

    Article  Google Scholar 

  20. Bulman S, Braselton JP (2014) Rhizaria: Phytomyxea. In: McLaughlin DJ, Spatafora JW (eds) The Mycota VII Part A, Systematics and evolution2nd edn. Springer-Verlag, Berlin, pp 783–803

    Google Scholar 

  21. Feldmann G (1954) La végétation de l’etang de Salses (riv sud). Vie Milieu 4:685–700

    Google Scholar 

  22. Feldmann G (1956) Développement d’une plasmodiophorale marine: Plasmodiophora bicaudata J. Feldm., parasite du Zostera nana Roth. Revue Gen Bot 63:390–421

    Google Scholar 

  23. Lipkin Y (1975) Halophila stipulacea, a review of a successful immigration. Aquat Bot 1:203–215

    Article  Google Scholar 

  24. Marziano F, Villari R, Tripodi G (1995) A plasmodiophorid fungal parasite of the seagrass Halophila stipulacea. Mycotaxon 55:165–170

    Google Scholar 

  25. Vohník M, Borovec O, Özgür Özbek E, Okudan Alsan E (2017) Rare phytomyxid infection on the alien seagrass Halophila stipulacea in the southeast Aegean Sea. Mediterr Mar Sci 18:433–442

    Article  Google Scholar 

  26. Gambi MC, Barbieri F, Bianchi CN (2009) New record of the alien seagrass Halophila stipulacea (Hydrocharitaceae) in the western Mediterranean: a further clue to changing Mediterranean Sea biogeography. Mar Biodivers Rec 2:e84

    Article  Google Scholar 

  27. Gambi MC, Gaglioti M, Barbieri F (2018) Sometimes they come back: the re-colonization of the alien seagrass Halophila stipulacea (Forsskål) Ascherson, 1867 (Hydrocharitaceae) in the Palinuro Harbor (Tyrrhenian Sea, Italy). Bioinvasions Rec 7:215–221

    Article  Google Scholar 

  28. Feldmann J (1940) Une nouvelle espece de Plasmodiophora (P. bicaudata) parasite du Zostera nana Roth. Bull Soc Hist nat Afr Nord 31:171–177

    Google Scholar 

  29. Ferdinandsen, C, Winge Ö (1913) Plasmodiophora halophilae sp. n. Zentralblatt für Bakteriologie, Parasitenkunde, und Infektionskrankheiten 37:167

  30. Cook WRI (1933) A monograph of the Plasmodiophorales. Arch Protistenkd 80:179–254

    Google Scholar 

  31. Dick MW (2001) Straminopilous fungi: systematics of the peronsoporomycetes including accounts of the marine straminipilous protists, the plasmodiophorids and similar organisms. J Gen Virol 75:3585–3590

    Google Scholar 

  32. Goebel K (1884) Tetramyxa parasitica. Flora 67:517–521

    Google Scholar 

  33. Kornaś J (1953) Tetramyxa parasitica Goebel w zatoce Gdanśkiej. Fragm Flor et Geobot 1:12–15

    Google Scholar 

  34. den Hartog C (1963) Tetramyxa parasitica, een gal op Ruppia. Gorteria 1:138–140

    Google Scholar 

  35. Braselton JP (2019) Plasmodiophorid Home Page. https://people.ohio.edu/braselto/plasmodiophorids/. Accessed on 1st March 2019

  36. Famà P, Acunto S, Camilli L, Maltagliati F, Procaccini G (1999) Genetic variation in two Mediterranean populations of Halophila stipulacea (Forssk.) Aschers. Biol Mar Mediterr 6:184–190

    Google Scholar 

  37. Di Martino V, Blundo MC, Tita G (2006) The Mediterranean introduced seagrass Halophila stipulacea in eastern Sicily (Italy): temporal variations of the associated algal assemblage. Vie Milieu 56:223–230

    Google Scholar 

  38. Vohník M, Borovec O, Župan I, Vondrášek D, Petrtýl M, Sudová R (2015) Anatomically and morphologically unique dark septate endophytic association in the roots of the Mediterranean endemic seagrass Posidonia oceanica. Mycorrhiza 25:663–672

    Article  PubMed  Google Scholar 

  39. Medlin L, Elwood HJ, Stickel S, Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71(2):491–499

    Article  CAS  PubMed  Google Scholar 

  40. Marande W, López-García P, Moreira D (2009) Eukaryotic diversity and phylogeny using small-and large-subunit ribosomal RNA genes from environmental samples. Environ Microbiol 11(12):3179–3188

    Article  PubMed  Google Scholar 

  41. Elwood HJ, Olsen GJ, Sogin ML (1985) The small-subunit ribosomal RNA gene sequences from the hypotrichous ciliates Oxytricha nova and Stylonychia pustulata. Mol Biol Evol 2:399–410

    CAS  PubMed  Google Scholar 

  42. Katoh K, Misawa K, Kuma KI, Miyata T (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30(14):3059–3066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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 

  44. Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  46. Bignami F, Salusti E (1990) Tidal currents and transient phenomena in the Strait of Messina: a review. In: Pratt LJ (ed) The physical oceanography of sea straits. Springer, Dordrecht, pp 95–124

    Chapter  Google Scholar 

  47. Murúa P, Goecke F, Westermeier R, van West P, Küpper FC, Neuhauser S (2017) Maullinia braseltonii sp. nov. (Rhizaria, Phytomyxea, Phagomyxida): a cyst-forming parasite of the bull kelp Durvillaea spp. (Stramenopila, Phaeophyceae Fucales). Protist 168:468–480

    Article  PubMed  PubMed Central  Google Scholar 

  48. Willette DA, Chalifour J, Debrot AOD, Engel MS, Miller J, Oxenford HA et al (2014) Continued expansion of the trans-Atlantic invasive marine angiosperm Halophila stipulacea in the Eastern Caribbean. Aquat Bot 112:98–102

    Article  Google Scholar 

  49. Jiang R, Wang JX, Yu KC, Liu MH, Shi G, Liu XZ (2016) Micro-eukaryotic diversity in the surface layer of sediments from the East China Sea. Evol Ecol Res 17(1):125–140

    Google Scholar 

  50. Takishita K, Miyake H, Kawato M, Maruyama T (2005) Genetic diversity of microbial eukaryotes in anoxic sediment around fumaroles on a submarine caldera floor based on the small-subunit rDNA phylogeny. Extremophiles 9(3):185–196

    Article  CAS  PubMed  Google Scholar 

  51. Anonymous (2014) https://floramalesiana.biowikifarm.net/wiki/Jensen,_Hjalmar. Accessed on 7th December 2018

  52. Karling JS (1968) The Plasmodiophorales, Second completely revised edition. Hafner Publishing Company, New York

    Google Scholar 

  53. Tur NM, Vobis G, Gabellone NA (1984) Presencia de Tetramyxa parasitica (Plasmodiophoraceae) en dos especies de Potamogeton (Potamogetonaceae). Revista del Museo de La Plata (nueva serie). Sección Botánica 13(82):239–246

    Google Scholar 

  54. Buczacki ST, Ockendon JG (1978) A method for the extraction and enumeration of resting spores of Plasmodiophora brassicae from infested soil. Ann Appl Biol 88:363–367

    Article  Google Scholar 

  55. Takahashi K, Yamaguchi T (1987) An improved method for estimating the number of resting spores of Plasmodiophora brassicae in soil. Ann Phytopath Soc Japan 53:507–515

    Article  Google Scholar 

  56. Walker AK, Campbell J (2009) First records of the seagrass parasite Plasmodiophora diplantherae from the Northcentral Gulf of Mexico. Gulf Caribb Res 21:63–65

    Google Scholar 

  57. Elliott JK, Simpson H, Teesdale A, Replogle A, Elliott M, Coats K, Chastagner G (2019) A novel phagomyxid parasite produces sporangia in root hair galls of eelgrass (Zostera marina) 170:64–81

Download references

Acknowledgments

The authors acknowledge Gabriele Procaccini for the mediation of our cooperation in the beginning of this wonderful journey, Ondřej Borovec for the preparation of the permanent slides, Michael Kotyk for his help and brilliant ideas in the molecular procedures and Jiří Machač for the assistance during photographic documentation.

Funding

This study was supported by the Grant Agency of Charles University (project GAUK 1308218) and constitutes a part of long-term research projects of the Czech Academy of Sciences, Institute of Botany (RVO 67985939), and Charles University, Faculty of Science (MŠMT LO1417).

Author information

Authors and Affiliations

  1. Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic

    Viktorie Kolátková

  2. Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

    Ivan Čepička

  3. Department of Chemical, Biological, Pharmaceutical and Environmental Sciences, University of Messina, Messina, Italy

    Gaetano Maurizio Gargiulo

  4. Department of Mycorrhizal Symbioses, Institute of Botany, Czech Academy of Sciences, Průhonice, Czech Republic

    Martin Vohník

  5. Department of Experimental Plant Biology, Faculty of Science, Charles University, Prague, Czech Republic

    Martin Vohník

Authors
  1. Viktorie Kolátková
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ivan Čepička
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gaetano Maurizio Gargiulo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martin Vohník
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Viktorie Kolátková.

Electronic supplementary material

ESM 1

(FAS 70 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolátková, V., Čepička, I., Gargiulo, G.M. et al. Enigmatic Phytomyxid Parasite of the Alien Seagrass Halophila stipulacea: New Insights into Its Ecology, Phylogeny, and Distribution in the Mediterranean Sea. Microb Ecol 79, 631–643 (2020). https://doi.org/10.1007/s00248-019-01450-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-019-01450-3

Keywords

Search

Navigation