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Bryology and Lichenology |
2Centro de Ciencias Medioambientales, C.S.I.C., Calle Serrano 115 bis, 28006 Madrid, Spain; 3University Herbarium, University of California, Berkeley, California 94720-2465 USA
Received for publication August 14, 2003. Accepted for publication December 4, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: haustoria • marine lichen • mycophycobiosis • Petroderma maculiforme • Phaeophyceae • phycobiont • pyrenomycetes • Verrucaria tavaresiae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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) is the only fungus reported to form a lichen association with a brown alga (Phaeophyceae). The phycobiont isolated from the symbiotic thallus was identified as Petroderma maculiforme (Wollny) Kuckuck (Wynne, 1969
). This result was subsequently confirmed by morphological and molecular comparison of algal isolates with material cultured from type locality collections (Peters and Moe, 2001
).
Free-living Petroderma maculiforme produces a small discoid thallus of appressed radial filaments, the cells of which give rise to a cushion of laterally coherent, erect filaments (Edelstein and McLachlan, 1969
; Wilce et al., 1970
). Although relatively simple compared to many other brown algae, this species would nonetheless be among the most structurally complex of algae known to enter into lichen symbioses. Most other lichen phycobionts are unicellular or short-filamentous microalgae (Tschermak-Woess, 1988
).
On the other hand, there are a few apparently obligate symbioses between ascomycete fungi and complex macroalgae that have generally not been treated as lichens. For example, the ubiquitous association of the fungus Mycophycias ascophylli with the phaeophycean rockweed Ascophyllum nodosum has been termed a mycophycobiosis rather than a lichen (Kohlmeyer and Kohlmeyer, 1972
; Kohlmeyer and Volkmann-Kohlmeyer, 1998
). The distinction was made on the grounds that the microscopic fungus in that association merely invades the tissues of the seaweed without engendering any morphological transformation or construction of a distinctive thallus.
Taking these different partnerships into account, Moe (1997)
indicated that the Verrucaria tavaresiae–Petroderma maculiforme symbiosis should be considered a lichen. However, no structural study of this unique association has yet been published, despite repeated citation of the thesis in which it was first mentioned decades ago (Wynne, 1969
). The neglect of these organisms is particularly surprising in view of their presence on the urbanized shores of cosmopolitan San Francisco Bay (California, USA). The present work investigates the organization of their symbiotic thallus and the types of cellular contacts between symbionts, providing evidence regarding the status of the association as a lichen.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Asensi et al., 1977
). However, the symbiotic thallus it forms in association with the fungus Verrucaria tavaresiae is known only from maritime northern and central California, USA (Wynne, 1969
; Moe, 1997
; Tucker, 1999
).
Light microscopy
Hand sections of Verrucaria tavaresiae were prepared from material collected from the middle-upper intertidal zone in San Francisco Bay (Treasure Island and Fort Mason, San Francisco County) and on the Pacific coast at McClure's Beach (Marin County), California, USA. Thalli were growing on sandstone rock faces with a northern exposure. Voucher specimens are deposited at the University Herbarium, Berkeley (UC).
Electron microscopy
As lichen material has often proven difficult to process adequately for transmission electron microscopy (TEM), we used a microwave-assisted protocol for fixation and embedding, developed by the Electron Microscopy Laboratory of the University of California at Berkeley. Specimens collected at Fort Mason were kept moist with seawater and processed within 24 h at the EM Laboratory in Berkeley. The thallus was cut transversely into sections approximately 2 x 1 x 0.3 mm. Material was fixed in glutaraldehyde diluted to 2% with seawater, postfixed with osmium tetroxide, dehydrated in acetone series, and embedded in Spurr's low-viscosity resin. Fixation, dehydration, and embedding were carried out under vacuum within a laboratory-adapted microwave oven (Ted Pella) provided with a water- cooled specimen pedestal. A restriction temperature of 35°C (above which the microwave automatically shuts off) was employed. Ultrathin sections were prepared with an Ultracut E microtome (Reichert-Jung) and examined with a Leo 910 transmission electron microscope (Zeiss) at the Centro de Ciencias Medioambientales, C.S.I.C, in Madrid.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Margins of the thallus
Along the perimeter of the symbiotic thallus, a narrow prothallus of fungal tissue (Fig. 2) adhered closely to the substrate and was difficult to dislodge intact for examination. Within the fungal tissue just proximal to the prothallus, the phycobiont was present as a single layer of algal filaments oriented parallel to the surface (Fig. 15). With increasing distance from the margin, the cells of the horizontal filament system became increasingly separated from each other. Some sections show filament growth becoming oblique and disorganized, then increasingly anticlinal in orientation (Fig. 16); others show periclinal divisions (= new crosswalls parallel to surface) giving rise to anticlinal files of algal cells (Figs. 17–18). About 500–1000 µm from the prothallic margin, the algal layer assumed its mature structure, with most algal filaments fully anticlinal and distinctly separated from each other by surrounding fungal cells (Fig. 19).
Reproductive structures of the mycobiont
Pycnidia developed at the thallus surface beneath a dense superficial deposit of pigmentation (Fig. 20). The pycnoconidia were filiform. Ascomatal primordia similarly developed below pigmented superficial cells. Cells of distinctive morphology, densely staining in lactophenol-cotton blue, were observed in the center of the primordia; these cells appeared to form part of an ascogonial complex (Fig. 21). A dense ring of dark pigmentation surrounded the ostiole of the mature perithecium. The inner surface of the perithecial neck was lined with periphyses (Fig. 22). The mature hymenium lacked interascal filaments. Asci were club-shaped; ascospores ovoid, simple, eight per ascus, 12–15 x 5–7 µm (Fig. 23). Further details of reproductive characters are provided by Moe (1997)
.
Ultrastructure of fungal and algal symbionts
Intimate symbiont contact was evident throughout the algal layer, where fungal and algal walls were in continuous apposition (Fig. 24). The algal cell wall was more distinctly delimited, substantially more electron-dense, and had a definite layered structure. Algal filament crosswalls were traversed by plasmodesmata. The chloroplast often occupied much of the algal cell volume. They were frequently lobed, varying substantially in discernable shape and orientation. A large central pyrenoid was often conspicuous, with chloroplast lobes folded around it (Fig. 24). An invagination of the chloroplast membrane ramified throughout the pyrenoid, forming a network of branched tubules (Fig. 25; see also Asensi et al., 1977
). Although chloroplast number could not be determined with certainty from nonserial sections, one chloroplast per cell seemed to be the most common condition. Sometimes, the presence of two separate chloroplasts per cell could be confirmed when the central pyrenoids of both were clearly visible (Fig. 27). Plastoglobuli were generally absent from the pyrenoid, but occurred in short rows or clusters within dilations of stroma between the lamellae (Fig. 25). Mitochondria were conspicuous and abundant in many of the algal cells (Fig. 24). Further details of Petroderma ultrastructure will be presented in a separate work comparing the lichenized and free-living states.
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Cells of the medulla tended to be more irregularly shaped or even hypha-like. The intercellular matrix material in this zone was electron-dense and readily disinguishable from the fungal cell wall proper (Figs. 30–32). Within many medullary cells, large, electron-dense, lipid-like globules, generally not associated with a vacuolar system, occupied a substantial portion of the protoplast volume (Fig. 30). Intrahyphal hyphae were common (Fig. 30), invasion occurring between adjacent cells of the same hypha (Fig. 31). Anastomoses between adjacent hyphae occurred frequently (Fig. 32).
Contacts and interactions between symbionts
Intraparietal haustoria-like structures were commonly observed. These were peglike protrusions of the fungal cell wall that penetrated into an adjacent algal cell wall (Figs. 33–38). The protrusions generally appeared in section as solid wall material (Fig. 33), with no more than a slight corresponding protrusion of the fungal protoplast at the base (Fig. 34), but without any central strand of protoplasm detectable within. The depth of penetration and thinning of the algal wall varied; in a number of cases, the algal wall was nearly traversed, but in no instance were fungal structures seen to enter the algal cell lumen. Frequently, a substantial delamination of the algal cell wall was evident around the haustorium-like structure, with fungal wall material penetrating between the separated layers of algal wall (Figs. 35–38). Conversely, the downward growth of the algal filaments involved a reciprocal penetration through the fungal tissue. The terminal cells of the algal filaments typically became narrow and sinuous apically as they forced their way through the wall material between fungal cells (Fig. 39). These intrusions of the algal filaments could penetrate deeply into the fungal cell wall, which often was substantially thinner at such contact points (Figs. 40–42). In some cases, a proliferation of cytoplasmic membranes was notable in the fungal protoplast adjacent to these contacts (Fig. 42).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). The ochrophytes also include the Xanthophyceae, of which one member (Heterococcus caespitosus) has also been reported as phycobiont in three species of Verrucaria lichens (Tschermak, 1941
; Zeitler, 1954
; Parra and Redón, 1977
). Together with certain heterotrophic organisms such as the oomycetes, the ochrophyte algae may be placed within a distinct kingdom denominated Chromista (Cavalier-Smith, 1998
) or Straminipila (Dick, 2001
). Petroderma and Heterococcus are thus very different phylogenetically from both the chlorophyte and cyanophyte algae that serve as phycobionts in all other known lichen associations.
Despite the distinctive nature of the phycobiont, Verrucaria tavaresiae and Petroderma maculiforme form a lichen thallus with an organization comparable to that of many other crustose lichens. Within a cellular tissue formed by the fungus, Petroderma is transformed into a discrete layer of separate, downward-growing filaments. Thus, the growth properties of both filamentous fungus and multicellular alga are profoundly altered in symbiosis. The cytological characteristics of the mycobiont are quite similar to those described in other ascomycete lichens. Fungal cell walls are "gelatinized" or confluent in an apparent matrix, and their protoplasts show a conspicuous vacuolar system with osmiophilic contents reminiscent of those reported in other lichens (Boissière, 1979
, 1982
). The fungal cytoplasm contains concentric bodies, a feature observed in most lichenized ascomycetes that have been studied ultrastructurally. The significance of these structures is still unclear, but their occurrence seems to be correlated with fungi subject to drought stresses (Honegger, 1993
). Their presence in V. tavaresiae, which colonizes an intertidal habitat, is certainly compatible with this pattern. The diurnal alternation between full immersion and exposure probably causes considerable mechanical stress on the thallus tissue. Cracking of the thallus upon drying often occurs along the pigmented markings of the upper thallus layers, as previously reported in another maritime Verrucaria species, V. degelii (Santesson, 1939).
The cellular contacts between the symbionts have distinctive structural features. While so-called intraparietal haustoria are typical of many lichens, the observed separation of algal wall layers and insertion of fungal wall material between them does not appear to have been reported previously. The reciprocal penetration by intrusive growth of the algal filaments into the fungal walls is another striking feature of this symbiosis. These elaborate interpenetrations between symbionts might provide increased integration of cells within a tissue that is subject not only to the mechanical stresses of hydric extremes, but also to the markedly divergent cellular growth patterns of its two biological components.
Inferred model of thallus growth
Because the crustose thallus of V. tavaresiae is intimately attached to the substratum, radial growth must take place at the thallus margin, where stages in thallus development are observable. The periclinally oriented filaments of the phycobiont present at the thallus margin are interpenetrated by fungal cells and reorganized into short, separate, anticlinally oriented filaments. Several observations indicate that the growth of these anticlinal algal filaments is primarily downward into the fungal tissue: (1) branches of the lichenized algal filaments are usually oriented downward; (2) the lowermost cells of the filaments grow intrusively between the cells of the fungal tissue below; and (3) the uppermost cells of the algal filaments are often moribund and physically eroded, as are those of adjacent fungal cells. Compared to the erect filaments of the free-living Petroderma, the lichenized algal filaments appear to have the reverse polarity of growth. The growth of the phycobiont downward into the fungal tissue permits the algal layer to maintain its position among the periclinally dividing fungal cells while regenerating algal cells to replace those sloughed off at the upper surface of the thallus.
The arrangement of fungal cells in files, with mainly periclinal crosswalls visible, indicates considerable production of fungal tissue perpendicular to the surface of the thallus. These cell divisions appear to be most concentrated within a region comprising the lower algal layer and upper subalgal layer. Several observations support this interpretation: (1) Fungal cells in this region tend to be smaller, thinner-walled, and arranged in anticlinal files with mostly periclinal crosswalls evident. (2) The cytoplasm of the cells in this zone stain most densely with aniline blue (Figs. 9, 19), suggesting intense metabolic activity. (3) The highly electron-dense globules associated with vacuoles in the algal and subalgal layers often appear markedly smaller in the lower algal and upper subalgal region, suggesting mobilization of resources by these cells for growth processes (Figs. 10–11, 26). The subsurface cell divisions may provide for the renewal of fungal tissue removed by abrasion of the surface through wave action and the scouring effect of suspended particles, analogous to the basal replacement of grazed leaf tissue by intercalary meristems in grasses. Herbivory by intertidal organisms, an important factor in the ecology of many intertidal plants, may also contribute significantly to removal of surface tissues in Verrucaria tavaresiae (Fig. 2).
Fungal–algal contacts
Previous workers described symbiont interactions in other species of Verrucaria. With light microscopy, Tschermak (1941)
observed tiny intraparietal haustoria in Verrucaria nigrescens Pers. and related Dermatocarpon species, but reported an absence of penetrating structures in the lichen formed by Verrucaria elaeomelaena (= V. funckii according to Tschermak-Woess, 1988
) and its thin- walled xanthophycean phycobiont Heterococcus. Tschermak (1941
: fig. 7n, p) also discerned pairs of closely spaced penetrating structures in V. nigrescens; their resolution must have approached the limits of the light microscope. Such closely adjacent penetrations were not observed in the present study of V. tavaresiae, although they were apparent in electron micrographs of other Verrucaria species examined by Galun et al. (1973
: fig. 2) and Kushnir and Galun (1977
: fig. 5). Those authors claimed that in haustorial interactions of pyrenocarpous lichens such as Dermatocarpon and Verrucaria, the fungal cell wall as well as the algal wall disintegrate, and a naked fungal protoplast emerges toward the algal cell. This conclusion appeared to be based on micrographs in which an electron-transparent area exterior to the fungal protoplast was interpreted as a "space" (fig. 4 in Galun et al., 1971
; figs. 2–3 in Kushnir and Galun, 1977
). However, the electron-transparent areas in question may actually correspond to the fungal cell wall. In the present study, no dissolution of fungal wall was observed where the algal cell wall was penetrated, although the fungal wall was thinner where intrusively growing algal filaments pushed downward against the fungal cells below them (Figs. 40–42). The deeply penetrating, intracellular fungal haustoria seen within the algal cell lumen in a number of pyrenolichens growing on bark (Matthews et al., 1989
) and leaves (Chapman, 1976
) were not observed in V. tavaresiae.
In general, the structurally primitive crustose thalli with unstratified organization tend to have deeply penetrating intracellular haustoria, while the more structurally advanced crustose, foliose, and fruticose lichens have either non-penetrative contacts between symbionts or intraparietal penetrations that do not enter the algal cell lumina (Tschermak, 1941
; Plessl, 1963
; Honegger, 1986
). Verrucaria tavaresiae appears consistent with this general pattern. Within its stratified, highly organized thallus, penetration of the phycobiont is limited to intraparietal protrusions of the mycobiont wall. In certain lichens, the type of symbiont contact may also be influenced by structural features of particular algal symbionts. For example, the lack of wall penetration in lichens containing the phycobiont Coccomyxa (Tschermak, 1941
; Peveling and Galun, 1976
) might be explained by the presence of degradation-resistant polymers in the algal cell wall (Brunner and Honegger, 1985
; Honegger, 1988
). In V. tavaresiae, the delamination of the algal wall near points of fungal penetration might be at least partly attributable to structural characteristics peculiar to the phaeophyte cell wall.
Although lichen haustoria have been repeatedly studied, their function and significance are still not fully understood. While the term haustorium suggests a specialized absorptive structure, there is no evidence that lichen haustoria indeed play such a role. Neither autoradiographic studies with labeled carbohydrate (Jacobs and Ahmadjian, 1971
; Hessler and Peveling, 1978
) nor calculations of carbohydrate movement between symbionts (Collins and Farrar, 1978
) have indicated any special relevance of lichen haustoria in the transfer of nutrients between symbionts. Clearly, the simple intraparietal haustoria present in many lichen thalli do not substantially increase the surface area of contact between the symbiont protoplasts, as do the branching, intracellular haustoria typical of plant parasites and endomycorrhizae. In V. tavaresiae, the fungal penetration pegs are protruding wall material usually without fungal protoplasm, further undermining speculation that these structures might facilitate transfer of materials. Their function may well be more structural than nutritional. The laterally penetrating flanges lock the fungal penetration pegs within the algal wall, impeding separation of the contacting symbiont cell surfaces. The converse penetration of algal filaments into the fungal cell wall may further help bind the symbiont cells together. These reciprocal penetrations may thus facilitate the coherence and integration of unlike cellular elements, much as the anastomoses that bind like cells of adjacent filaments (Fig. 32) play an important role in the construction of a pseudoparenchyma (Poelt, 1986
). This may be of particular significance in lichen tissues subject daily to mechanical stresses of extreme hydration and dehydration. In growth zones of lichens containing the unicellular phycobiont Trebouxia, a related role in integrating or coordinating symbiont growth in morphogenesis has been attributed to the penetrative hyphae that separate and shift dividing algal cells (Greenhalgh and Anglesea, 1979
; Honegger, 1987
). Thus, the originally absorptive, nutritional function of intracellular haustoria in primitive lichens may have evolved into a more structural/mechanical role, allowing dividing algal cells to be more closely coordinated or shifted with fungal growth and thereby permitting the construction of more highly organized lichen thalli.
Ecological and reproductive considerations
Although reports of the diminutive and easily overlooked Petroderma are scanty, the microhabitat preferences of the independent alga appear to be distinct from those of the lichenized form. Free- living P. maculiforme is not very tolerant of strong wave action nor of desiccation (Wilce et al., 1970
). It occupies the lowermost regions of the intertidal zone, except where protected moist crevices permit it to colonize higher, and frequently occurs submerged in tidal pools (Edelstein and McLachlan, 1969
; Fletcher, 1987
). In San Francisco Bay, free- living Petroderma was most readily found on discarded plastic among rocks and sand exposed only at very low tide at the calmer East Bay shore. Lichen symbiosis with Verrucaria tavaresiae therefore appears to extend the alga's range into more exposed microhabitats subject to vigorous wave action and more extreme desiccation. On the other hand, the lichenized Petroderma populations have not been observed to form reproductive structures. Nor does the lichen bear any recognizable type of vegetative propagule that includes the algal symbiont. Verrucaria tavaresiae appears to reproduce via ascospores, which after dispersal and germination must relichenize Petroderma germlings or zoospores originating from free-living algal thalli. Established Petroderma thalli probably do not become lichenized, as the lichen does not appear to thrive where the free-living alga does.
This situation appears to contrast with that of the lichen Strigula, which can colonize leaves bearing the reproductively mature, free-living thalli of its phycobiont Cephaleuros (see fig. 4 in Sanders, 2001
). According to Ward (1884)
, the germinating spores of Strigula complanata (= S. orbicularis) consume rather than lichenize very young Cephaleuros thalli and can only form stable lichen symbioses when algal thalli in more advanced stages of development are contacted. The comparison is of interest because Cephaleuros (Trentepohliaceae) is perhaps the only known lichen phycobiont equivalent in structural complexity to Petroderma.
The complete suppression of algal reproduction and dispersal after lichenization would seem unlikely, because occasional phycobiont "escape" and sexual recombination are necessary for symbiotic coevolution. The level of thallus organization and lack of apparent parasitism of the algal cells indicate that this lichen symbiosis is indeed stable and highly coevolved. It is possible that Petroderma might regenerate and reproduce free-living from abraded lichen fragments in nature as it readily does in culture (Peters and Moe, 2001
) or indeed produce zooangia on lichenized filaments under certain conditions or at certain times of the year. However, a molecular comparison of lichenized Petroderma from California and free-living Petroderma from the type locality in the North Sea showed identical nuclear ribosomal ITS1 sequences; this highly variable gene typically differs between species and even populations in brown algae (Peters and Moe, 2001
). The suggestion of genetic uniformity between these widely separated populations is surprising, and it will be interesting to see if comparison of other informative genes gives similar results.
Lichens vs. mycophycobioses
Various authors have differed slightly in the characteristics they emphasize as definitive of a lichen symbiosis, as distinct from other types of fungal– algal symbioses. Hawksworth (1988)
stressed that the fungal component is the exhabitant, enclosing the algal symbiont, while Jahns (1988)
emphasized the formation of a distinctive thallus by the mycobiont. The Verrucaria tavaresiae–Petroderma maculiforme symbiosis clearly fits these definitions, distinguishing it from other known fungus–phaeophyte symbioses. Yet one might question whether the distinction of lichens from mycophycobioses is always made consistently and indeed whether this distinction is always biologically meaningful. For example, the Collemataceae include certain species of fungi with hyphae that simply penetrate the sheath material of Nostoc without forming any vegetative tissues or external cortex. It is hardly clear that these fungi should be considered exhabitants, nor that their thalli represent substantial morphological transformation when compared to macroscopic, free- living aggregates of Nostoc. Nonetheless, the status of these associations as lichens is not questioned, while those formed by Mycophycias with seaweeds have been treated distinctly. Conversely, the glomalean fungus Geosiphon pyriforme alters its hyphal morphology to produce bladder-like swellings in the presence of its algal symbiont, and the fungus is clearly the exhabitant (the alga is actually enclosed within the fungal cell lumina; Schüßler and Kluge, 2001
), yet this association is not considered to be a lichen. In practice, the boundaries we give to the lichen concept may actually be influenced by the perceived biosystematic affiliations of the fungi involved. If Geosiphon pyriforme or Mycophycias ascophylli were closely related to other fungal taxa known to form typical lichen thalli, it is likely that we would consider them also to be lichens and modify our definitions accordingly. The same would surely apply to the Turgidosculum complicatulum–Prasiola crispa association, whose status as a lichen (Lamb, 1948
) may still face some lingering doubts (Lud et al., 2001
). In the case of Mycophycias and its seaweed hosts, a close ecological correspondence with lichen symbioses might be implied by obligatory co-occurrence, as well as by data suggesting improved algal host growth (Garbary and MacDonald, 1995
) and tolerance of desiccation (Garbary and London, 1995
). In this regard it is worth mentioning that recent taxonomic placement of the genus Mycophycias in the Verrucariales (Kohlmeyer and Volkmann-Kohlmeyer, 1998
) suggests the possibility of a closer phylogenetic relationship with lichenized taxa such as Verrucaria, a hypothesis worthy of further investigation. However, the structural criteria that at present figure prominently in our definition of a lichen clearly place Verrucaria tavaresiae among the lichens while excluding Mycophycias ascophylli.
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FOOTNOTES |
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This work is dedicated to Dr. Isabelle I. Tavares, Curator Emerita of fungi and lichens at the University Herbarium (Berkeley) and namesake of the species V. tavaresiae, on the occasion of her 82nd birthday. 
4 E-mail: william{at}ccma.csic.es
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LITERATURE CITED |
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