The intertidal marine lichen formed by the pyrenomycete fungus Verrucaria tavaresiae (Ascomycotina) and the brown alga Petroderma maculiforme (Phaeophyceae): thallus organization and symbiont interaction

Abstract

The thallus formed by the marine pyrenomycete fungus Verrucaria tavaresiae and the phaeophycean alga Petroderma maculiforme was studied to elucidate the organization of the symbionts, determine the type of cellular contacts between them, and evaluate the status of the symbiosis as a lichen. Hand-sectioned and resin-embedded samples were examined with light and transmission electron microscopy. Within the uppermost portion of the cellular fungal tissue, separate algal filaments were arranged anticlinally. Protrusions of the fungal cell wall penetrated into adjacent algal walls but did not enter the cell lumen. A striking feature of these penetrations was the frequent separation of algal cell wall layers and insertion of fungal wall material between them. Algal filaments grew downward intrusively between fungal cells, often penetrating deeply into the fungal cell wall. Despite the exceptional nature of the phycobiont involved, the Verrucaria tavaresiae-Petroderma maculiforme symbiosis unequivocally fits the prevailing concept of a lichen. The distinctive interpenetrations observed between symbionts may be related to the integration of their different growth forms within a coherent tissue regularly subject to mechanical stresses. Periclinal cell divisions within and just below the algal layer may serve to replenish surface tissues lost to abrasion and herbivory.

Revisiting photobiont diversity in the lichen family Verrucariaceae (Ascomycota)

“…Moe, a species associated with the brown alga Petroderma maculiforme, was recently shown to belong to the genus Wahlenbergiella (Gueidan et al, 2011). In this association, the algal filaments are also embedded within a thallus formed by the fungus (Sanders et al, 2004(Sanders et al, , 2005.…”

“…Amphibious Verrucariaceae from both saline and freshwater habitats have repeatedly been reported in association with Dilabifilum, a genus of Ulvophyceae (TschermakWoess, 1970(TschermakWoess, , 1976Thu¨s, 2002). In addition, the Verrucariaceae is the only mostly lichenized family to form associations with Xanthophyceae (Heterococcus caespitosus Vischer: Tschermak, 1941b;Zeitler, 1954;Parra & Redon, 1977;Tschermak-Woess, 1988;Thu¨s & Schultz, 2008), Phaeophyceae [Petroderma maculiforme (Wollny) Kuckuck: Moe, 1997;Peters & Moe, 2001;Sanders et al, 2004Sanders et al, , 2005; Ascophyllum nodosum (Linnaeus) Le Jolis and Pelvetia canaliculata (Linnaeus) Decaisne & Thuret: Kohlmeyer & Volkmann-Kohlmeyer, 1998] and Rhodophyta (Apophlaea sp. : Kohlmeyer & VolkmannKohlmeyer, 1998).…”

Identification of Phymatolithon lamii (Me. Lemoine) Y.M. Chamberlain 1991 following bleaching in the upper intertidal zone of the Minas Basin, Nova Scotia, Canada

“…This crust organism was also very similar in appearance to two genera of marine intertidal lichens: Verrucaria spp. [12,15,16] (especially Verrucaria calciseda [12] and similar species in the genus with white-gray, rather than black-gray thallus colouration and black apothecia [15,16]) and Pyrenocollema spp. (e.g., Pyrenocollema halodytes, which is known to encrust intertidal surfaces [15]).…”

“…The congeneric species Phymatolithon laevigatum, in contrast, occurs within the intertidal and subtidal zones [14], and as a result of this, bleached specimens of this species are often reported [14], but not with the particular and unusual morphology (Figures 2 and 3) observed for bleached P. lamii in the present study. This species resembled a number of different taxa when bleached, including some (e.g., marine lichens [15,16]) that would be new to the region [12,13], which necessitated the present study. This study appears to be the first record to the author's knowledge of P. lamii occurring in the upper intertidal zone of Atlantic Canada.…”

Ultrastructural study of the brown algaPetroderma maculiforme(Phaeophyceae) in the free-living state and in lichen symbiosis with the intertidal marine fungusVerrucaria tavaresiae(Ascomycotina)

“…The identity of the laboratory-isolated phycobiont was confirmed by morphological and molecular comparison to algal cultures derived from free-living, type locality collections of Petroderma maculiforme (Peters & Moe, 2001). A recent structural study described the organization of the symbionts and their cellular interactions, demonstrating that the association clearly fits the concept of a lichen (Sanders et al, 2004). By contrast, other known symbioses between phaeophytes and ascomycete fungi have been treated as 'mycophycobioses' rather than lichens.…”