The formation of aegagropiles from the Mediterranean seagrass Posidonia oceanica (L.) Delile (1813): plant tissue sources and colonisation by melanised fungal mycelium
[en] Aegagropiles are conglomerations of fibre debris from Posidonia oceanica meadows that are frequently found along Medi- terranean beaches, but the plant organ from which these fibres arise remains unknown. In this study, a histological compari- son of P. oceanica organs from 3 shoots with the structure of aegagropile fibres showed that most of them arise from leaf sheaths and rhizomes, suggesting that they are degradation products from the “matte” rather than from the leaf litter, which is mainly composed of detached leaf blades. Moreover, fungal hyphae, micro-sclerotia and typical degradation traces were found in the peripheral tissues of living P. oceanica organs, as well as in degrading aegagropiles. We assume, by comparing Vohník’s observations and the observations made in this study, that these endophytic fungi and degradation traces might be attributed to a dark septate endophyte (DSE) in the Aigialaceae (Pleosporales), Posidoniomyces atricolor, which was recently described as an endosymbiont in P. oceanica roots. It constitutes one of the most important microorganisms by abundance that degrade P. oceanica tissues within the matte and give rise to the different fibre types in aegagropiles. This study shows that the proliferation of fungi causes organ degradation in Posidonia, starting early in living P. oceanica plants, continuing in the matte and, probably, in the leaf litter. The DSE plays a much more important role than that of a simple plant endosym- biont; its omnipresence within P. oceanica (and the degradation of the middle lamella and cell death during proliferation) causing the degradation of various Posidonia organs also contributes to the enrichment of the ‘matte’ compartment of this ecosystem, notably favouring nitrogen retention in its chitinous walls.
Lefebvre, Laurence ; Université de Liège - ULiège > Freshwater and OCeanic science Unit of reSearch (FOCUS)
Compère, Philippe ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution
Gobert, Sylvie ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Language :
English
Title :
The formation of aegagropiles from the Mediterranean seagrass Posidonia oceanica (L.) Delile (1813): plant tissue sources and colonisation by melanised fungal mycelium
Abadie A, Borges AV, Champenois W, Gobert S (2017) Natural patches in Posidonia oceanica meadows: the seasonal biogeochemical pore water characteristics of two edge types. Mar Biol 164:1–13. 10.1007/s00227-017-3199-5 DOI: 10.1007/s00227-017-3199-5
Addy HD, Piercey MM, Currah RS (2005) Microfungal endophytes in roots. Can J Bot 83:1–13 DOI: 10.1139/b04-171
Alva P, McKenzie EHC, Pointing SB, Pena-Muralla R, Hyde KD (2002) Do seagrasses harbor endophytes? In: Hyde KW (ed) Fungi in marine environments. Fungal diversity research series 7. Fungal Diversity Press, pp 167–178
Borovec O, Vohník M (2018) Ontogenetic transition from specialized root hairs to specific root-fungus symbiosis in the dominant Mediterranean seagrass Posidonia oceanica. Sci Rep 8:1–11. 10.1038/s41598-018-28989-4 DOI: 10.1038/s41598-018-28989-4
Borum J, Sand-Jensen K, Binzer T, Pedersen O, Greve TM (2006) Oxygen movement in seagrasses. Seagrasses Biol Ecol Conserv. 10.1007/978-1-4020-2983-7_10 DOI: 10.1007/978-1-4020-2983-7_10
Boudouresque C-F, Meinesz A (1982) Découverte de l’herbier de Posidonies. In: Cahier du Parc National de Port-Cros, pp 1–79
Boudouresque CF, Crouzet A, Pergent G (1983) Un nouvel outil au service de l’étude des herbiers à Posidonia oceanica: la lepidochronologie. Rapp PV Réun Comm Int Pour L’explor Sci Entifique De La Méditerr 28:111–112
Boudouresque C-F, Bernard G, Bonhomme P, Charbonnel E, Diviacco G, Meinesz A, Pergent G, Pergent-Martini C, Ruitton S, Tunesi L (2012) Protection and conservation of Posidonia oceanica meadows. RAMOGE and RAC/SPA publisher
Brodersen KE, Kühl M, Nielsen DA, Pedersen O, Larkum AWD (2018) Rhizome, root/sediment interactions, aerenchyma and internal pressure changes in seagrasses. Seagrasses Aust Struct Ecol Conserv. 10.1007/978-3-319-71354-0_13 DOI: 10.1007/978-3-319-71354-0_13
Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev Camb Philos Soc 79:473–495 DOI: 10.1017/S1464793103006316
Brundrett MC (2009) Mycorrhizal associations and other means of nutrition of vascular plants: understanding the global diversity of host plants by resolving conflicting information and developing reliable means of diagnosis. Plant Soil 320:37–77 DOI: 10.1007/s11104-008-9877-9
Cambridge ML, Kuo J (1979) Two new species of seagrasses from Australia, Posidonia sinuosa and P. angustifolia (posidoniaceae). Aquat Bot 6:307–328. 10.1016/0304-3770(79)90071-8 DOI: 10.1016/0304-3770(79)90071-8
Campbell NA, Reece JB (2004) Biologie. De Boeck. Adapté par Mathieu R, p 1482
Caye G, Rossignol M (1983) Etude des variations saisonnières de la croissance des feuilles et des racines de Posidonia oceanica. Mar Biol 75:79–88. 10.1007/BF00392633 DOI: 10.1007/BF00392633
Connell EL, Colmer TD, Walker DI (1999) Radial oxygen loss from intact roots of Halophila ovalis as a function of distance behind the root tip and shoot illumination. Aquat Bot 63:219–228. 10.1016/S0304-3770(98)00126-0 DOI: 10.1016/S0304-3770(98)00126-0
Debeir O, Allard J, Decaestecker C, Hermand J-P (2019) Characterization of Posidonia Oceanica seagrass aerenchyma through whole slide imaging: a pilot study. arXiv:1903.03044
Diaz-Almela E, Marbà N, Duarte CM (2007) Consequences of Mediterranean warming events in seagrass (Posidonia oceanica) flowering records. Glob Chang Biol 13:224–235 DOI: 10.1111/j.1365-2486.2006.01260.x
Eberl R (2011) Mycorrhizal association with native and invasive cordgrass Spartina spp. in San Francisco Bay, California. Aquat Biol 14:1–7 DOI: 10.3354/ab00378
Ganong WF (1905) On balls of vegetable matter from Sandy Shores. Rhodora 7:41–47
Giraud G (1979) Sur une méthode de mesure et de comptage des structures foliaires de Posidonia oceanica (Linnaeus) Delile. Bull Mus Hist Nat Marseille Fr 39:33–39
Gnavi G, Ercole E, Panno L, Vizzini A, Varese GC (2014) Dothideomycetes and Leotiomycetes sterile mycelia isolated from the Italian seagrass Posidonia oceanica based on rDNA data. Springerplus 3:508. 10.1186/2193-1801-3-508 DOI: 10.1186/2193-1801-3-508
Grünig CR, Queloz V, Sieber TN, Holdenrieder O (2008) Dark septate endophytes (DSE) of the Phialocephala fortinii s.l. - Acephala applanata species complex in tree roots: classification, population biology, and ecology. Botany 86:1355–1369 DOI: 10.1139/B08-108
Hayat M (1993) Stains and cytochemical methods. Plenum Publishing Corporation, New York, London
Holmer M, Duarte CM, Marbá N (2003) Sulfur cycling and seagrass (Posidonia oceanica) status in carbonate sediments. Biogeochemistry 66:223–239. 10.1023/B:BIOG.0000005326.35071.51 DOI: 10.1023/B:BIOG.0000005326.35071.51
Hosogi N, Nishioka H, Nakakoshi M (2015) Evaluation of lanthanide salts as alternative stains to uranyl acetate. Microscopy 64:429–435. 10.1093/JMICRO/DFV054 DOI: 10.1093/JMICRO/DFV054
Hurka H (1971) Factors influencing the gas composition in the vesicles of Sargassum. Mar Biol 11:82–89. 10.1007/BF00348024 DOI: 10.1007/BF00348024
Jensen SI, Kühl M, Glud RN, Jørgensen LB, Priemé A (2005) Oxic microzones and radial oxygen loss from roots of Zostera marina. Mar Ecol Prog Ser 293:49–58. 10.3354/meps293049 DOI: 10.3354/meps293049
Jones EBG, Pang K-L (2012) Marine fungi and fungal-like organisms. Walter de Gruyter & Co, Berlin, p 532 DOI: 10.1515/9783110264067
Kohlmeyer J, Volkmann-Kohlmeyer B (1991) Illustrated key to the filamentous marine fungi. Bot Mar 34:1–61. 10.1515/botm.1991.34.1.1 DOI: 10.1515/botm.1991.34.1.1
Kohlmeyer J, Volkmann-Kohlmeyer B (2001) The biodiversity of fungi on Juncus roemerianus. Mycol Res 105:1411–1412. 10.1017/S095375620124547X DOI: 10.1017/S095375620124547X
Kohlmeyer J, Volkmann-Kohlmeyer B (2002) Fungi on Juncus and Spartina: new marine species of Anthostomella, with a list of marine fungi known from Spartina. Mycol Res 106:365–374. 10.1017/S0953756201005469 DOI: 10.1017/S0953756201005469
Kohout P, Sýkorová Z, Čtvrtlíková M, Rydlová J, Suda J et al (2012) Surprising spectra of root-associated fungi in submerged aquatic plants. FEMS Microbiol Ecol 80:216–235 DOI: 10.1111/j.1574-6941.2011.01291.x
Kothamasi D, Kothamasi S, Bhattacharyya A, Kuhad RC, Babu CR (2006) Arbuscular mycorrhizae and phosphate solubilising bacteria of the rhizosphere of the mangrove ecosystem of Great Nicobar island, India. Biol Fertil Soils 42:358–361 DOI: 10.1007/s00374-005-0035-8
Kuo J (2007) Processing plant tissues for ultrastructural study. Methods Mol Biol 369:35–46
Kuo J, Cambridge ML (1978) Morphology, anatomy and histochemistry of the Australian seagrasses of the genus Posidonia könig (posidoniaceae). II. Rhizome and root of Posidonia australis Hook. F. Aquat Bot 5:191–206 DOI: 10.1016/0304-3770(78)90061-X
Kuo J, den Hartog C (2007) Seagrass morphology, anatomy, and ultrastructure. In: Larkum AWD, Orth RJ, Duarte CM (eds) Seagrasses: biology, ecology and conservation. Springer, Cham, pp 51–87
Kuo J, McComb AJ (1989) Seagrass taxonomy, structure and development. In: Larkum AWD, McComb AJ, Shephard SA (eds) Biology of seagrasses: a treatise on the biology of seagrasses with special reference to the Australian region. Elsevier Science Publications, Amsterdam, pp 6–73
Kuo J, McComb AJ, Cambridge ML (1981) Ultrastructure of the Seagrass Rhizosphere. New Phytol 89:139–143. 10.1111/j.1469-8137.1981.tb04756.x DOI: 10.1111/j.1469-8137.1981.tb04756.x
Larkum AWD, Orth RJ, Duarte CM (2006) Seagrasses: biology, ecology and conservation. Springer
Larkum AWD, Waycott M, Conran JG (2018) Evolution and biogeography of seagrasses. In: Larkum A, Kendrick G, Ralph P (eds) Seagrasses of Australia. Springer, Cham DOI: 10.1007/978-3-319-71354-0
Lefebvre L, Compère P, Léonard A, Plougonven E, Vandewalle N, Gobert S (2021) Mediterranean aegagropiles from Posidonia oceanica (L.) Delile (1813): a first complete description from macroscopic to microscopic structure. Mar Biol 168:1–17. 10.1007/s00227-021-03833-y DOI: 10.1007/s00227-021-03833-y
Lepot K, Compère P, Gérard E, Namsaraev Z, Verleyen E, Tavernier I, Hodgson DA, Vyverman W, Gilbert B, Wilmotte A, Javaux EJ (2014) Organic and mineral imprints in fossil photosynthetic mats of an East Antarctic lake. Geobiology 12:424–450. 10.1111/gbi.12096 DOI: 10.1111/gbi.12096
Mathieson AC, Hehre EJ, Dawes CJ (2000) Aegagropilous Desmarestia aculeata from New Hampshire. Rhodora 102:202–207
Mathieson AC, Dawes CJ, Lull WW (2015) Mystery beach balls foul Long Island, NY, beaches. Rhodora 117:92–97. 10.3119/14-11 DOI: 10.3119/14-11
Molenaar H, Barthélémy D, De Reffye P, Meinesz A, Mialet I (2000) Modelling architecture and growth patterns of Posidonia oceanica. Aquat Bot 66:85–99. 10.1016/S0304-3770(99)00071-6 DOI: 10.1016/S0304-3770(99)00071-6
Nicastro S, Innocenti AM, Passalacqua NG (2015) Histo-anatomical leaf variations related to depth in Posidonia oceanica. Funct Plant Biol 42:418–422. 10.1071/FP14111 DOI: 10.1071/FP14111
Nilsson T, Singh AP (2014) Tunnelling bacteria and tunnelling of wood cell walls, vol 1. McGraw-Hill, pp 395–399
Nielsen SL, Thingstrup I, Wigand C (1999) Apparent lack of vesiculararbuscular mycorrhiza (VAM) in the seagrasses Zostera marina L. and Thalassia testudinum Banks ex Konig. Aquat Bot 63:261–266 DOI: 10.1016/S0304-3770(98)00123-5
Olesen B, Enríquez S, Duarte CM, Sand-Jensen K (2002) Depth-acclimation of photosynthesis, morphology and demography of Posidonia oceanica and Cymodocea nodosa in the Spanish Mediterranean Sea. Mar Ecol Prog Ser 236:89–97. 10.3354/meps236089 DOI: 10.3354/meps236089
Onoda Y, Westoby M, Adler PB, Choong AMF, Clissold FJ, Cornelissen JHC, Díaz S, Dominy NJ, Elgart A, Enrico L, Fine PVA, Howard JJ, Jalili A, Kitajima K, Kurokawa H, McArthur C, Lucas PW, Markesteijn L, Pérez-Harguindeguy N, Poorter L, Richards L, Santiago LS, Sosinski EE, Van Bael SA, Warton DI, Wright IJ, Joseph Wright S, Yamashita N (2011) Global patterns of leaf mechanical properties. Ecol Lett 14:301–312 DOI: 10.1111/j.1461-0248.2010.01582.x
Ott JA (1980) Growth and production in Posidonia Oceanica (L.) Delile. Mar Ecol 1:47–64. 10.1111/j.1439-0485.1980.tb00221.x DOI: 10.1111/j.1439-0485.1980.tb00221.x
Pedersen O, Borum J, Duarte CM, Fortes MD (1998) Oxygen dynamics in the rhizosphere of Cymodocea rotundata. Mar Ecol Prog Ser 169:283–288. 10.3354/meps169283 DOI: 10.3354/meps169283
Pergent G, Pergent-Martini C (1990) Some applications of lepidochronological analysis in the seagrass Posidonia oceanica. Bot Mar 33:299–310. 10.1515/BOTM.1990.33.4.299/HTML DOI: 10.1515/BOTM.1990.33.4.299/HTML
Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Canadian Journal of Botany. NRC Research Press, Ottawa, pp 1074–1088
Radhika KP, Rodrigues BF (2007) Arbuscular mycorrhizae in association with aquatic and marshy plant species in Goa, India. Aquat Bot 86:291–294 DOI: 10.1016/j.aquabot.2006.10.009
Read DJ (1991) Mycorrhizas in ecosystems. Experientia 47:376–391 DOI: 10.1007/BF01972080
Read DJ (1999) Mycorrhiza: the state of the art. Mycorrhiza. Springer, Berlin, pp 3–34 DOI: 10.1007/978-3-662-03779-9_1
Remy F (2016) Characterization, dynamics and trophic ecology of macrofauna associated to seagrass macrophytodetritus accumulations (Calvi Bay, Mediterranean Sea). PhD thesis, p 285
Sanchez-Vidal A, Canals M, de Haan WP, Romero J (2021) Veny M (2021) Seagrasses provide a novel ecosystem service by trapping marine plastics. Sci Rep 111(11):1–7. 10.1038/s41598-020-79370-3 DOI: 10.1038/s41598-020-79370-3
Schmidt O, Bahmani M, Koch G, Potsch T, Brandt K (2016) Study of the fungal decay of oil palm wood using TEM and UV techniques. Int Biodeterior Biodegrad 111:37–44. 10.1016/j.ibiod.2016.04.014 DOI: 10.1016/j.ibiod.2016.04.014
Sculthorpe CD (1967) The biology of aquatic vascular plants. John Wiley & Sons Ltd, London
Sengupta A, Chaudhuri S (2002) Arbuscular mycorrhizal relations of mangrove plant community at the Ganges river estuary in India. Mycorrhiza 12:169–174 DOI: 10.1007/s00572-002-0164-y
Singh AP (2012) A review of microbial decay types found in wooden objects of cultural heritage recovered from buried and waterlogged environments. J Cult Herit 13:S16–S20. 10.1016/J.CULHER.2012.04.002 DOI: 10.1016/J.CULHER.2012.04.002
Sudová R, Rydlová J, Čtvrtlíková M, Havránek P, Adamec L (2011) The incidence of arbuscular mycorrhiza in two submerged Isoetes species. Aquat Bot 94:183–187 DOI: 10.1016/j.aquabot.2011.02.003
Tomlinson PB (1974) Vegetative morphology and meristem dependence: the foundation of productivity in seagrasses. Aquaculture 4:107–130. 10.1016/0044-8486(74)90027-1 DOI: 10.1016/0044-8486(74)90027-1
Torta L, Lo Piccolo S, Piazza G, Burruano S, Colombo P, Ottonello D, Perrone R, Di Maida G, Pirrotta M, Tomasello A, Calvo S (2015) Lulwoana sp., a dark septate endophyte in roots of Posidonia oceanica (L.) Delile seagrass. Plant Biol 17:505–511. 10.1111/plb.12246 DOI: 10.1111/plb.12246
Torta L, Burruano S, Giambra S, Conigliaro G, Piazza G, Mirabile G, Pirrotta M, Calvo R, Bellissimo G, Calvo S et al (2022) Cultivable fungal endophytes in roots, rhizomes and leaves of Posidonia oceanica (L.) Delile along the Coast of Sicily, Italy. Plants 11:1139. 10.3390/plants11091139 DOI: 10.3390/plants11091139
Trevisan M (2018) Recherche et caractérisation de symbioses microbiennes chimiosynthétiques ou digestives chez des crustacés amphipodes associés à des accumulations végétales en milieux marins côtier et profonds. Université de Liège
Vohník M (2021) Are lulworthioid fungi dark septate endophytes of the dominant Mediterranean seagrass Posidonia oceanica? Plant Biol. 10.1111/plb.13353 DOI: 10.1111/plb.13353
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. 10.1007/s00572-015-0642-7 DOI: 10.1007/s00572-015-0642-7
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. 10.1007/s00248-015-0640-5 DOI: 10.1007/s00248-015-0640-5
Vohník M, Borovec O, Župan I, Kolarík 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 Prog Ser 583:107–120. 10.3354/meps12337 DOI: 10.3354/meps12337
Vohník M, Borovec O, Kolaříková Z, Sudová R, Réblová M (2019) Extensive sampling and high-throughput sequencing reveal Posidoniomyces atricolor gen. Et sp. Nov. (Aigialaceae, Pleosporales) as the dominant root mycobiont of the dominant Mediterranean seagrass Posidonia oceanica. MycoKeys 55:59–86. 10.3897/mycokeys.55.35682 DOI: 10.3897/mycokeys.55.35682
Welsh AK, Burke DJ, Hamerlynck EP, Hahn D (2010) Seasonal analyses of arbuscular mycorrhizae, nitrogen-fixing bacteria and growth performance of the salt marsh grass Spartina patens. Plant Soil 330:251–266 DOI: 10.1007/s11104-009-0197-5