PHYCOBIONT FIDELITY IN UMBILICARIA

Dr. Steven L. Jessup
Southern Oregon University Herbarium

 
This study is designed to test symbiont specificity, or fidelity relationships, of phycobiont and mycobiont lineages in Western North American species of the lichen genus, Umbilicaria. Are mycobiont and phycobiont lineages within Umbilicaria associating at random, or is there some degree of specificity within and among lineages? If associations are non-random, to what extent can that pattern be explained by geographic codistribution of the symbionts? Is there a phylogenetic or coevolutionary component to the relationship? Only in recent years, with the development of DNA finger printing methods, has it become feasible to address these questions with a sample size adequate for the purpose. In this study I use inter-simple sequence repeat (ISSR) amplifications and gel analysis to identify phycobiont haplotypes and map their taxonomic distributions within and among taxa of associating mycobionts, and geographically in the ranges of several Western North American species of Umbilicaria.

Lichen bionts are, in many cases, largely or exclusively restricted in their spatial distribution to the lichen thallus. Both primary mycobionts and lichenicolous fungi, for example, are generally found in nature only on or in lichen thalli. While some photobionts, such as Trentepohlia and Nostoc, may commonly occur as freeliving organisms, other photobionts, such as Trebouxia and Pseudotrebouxia, are very rarely, if ever, found freeliving (Ahmadjian, 1988). Even those photobionts that are commonly found freeliving are found in many places only in association with lichen thalli.

Among the lichenicolous fungi there is a spectrum of specificity for the host lichen (Rambold and Triebel, 1992). Some lichenicolous fungi are found as saprobes as well as in the lichenicolous state. Others are completely restricted to lichen thalli, but occur on several lichen species. The marjority of lichenicolous fungi are narrowly restricted to one or a few lichen species (Honegger, 1996). It seems likely that, as with lichenicolous fungi, there exists a spectrum from very little specificity, or low fidelity, to highly specific, or high fidelity, in the relationship of phycobiont and mycobiont lineages. Ahmadjian (1993) lists sixteen species of Trebouxia and the lichens from which each has been isolated. T. irregularis, was reported from thirty different lichens. On the other hand, T. aymmetrica is reported from only one lichen species, Diploschistes albescens. Tschermak-Woess (1988) summarizes the lichen hosts of most known photobionts. The preponderance of evidence supports the conclusion that many if not most photobionts are capable of forming lichens with more than one mycobiont.

While it is undoubtedly true that some algae form lichens with more than one fungus, still relatively little is known about the fidelity, or host specificity of phycobiont lineages found in lichens within particular mycobiont lineages. Within particular lineages of mycobionts the question remains open whether and to what degree a particular fungal lineage is able to associate with more than one photobiont. Are the photobionts that are found within a lichen clade associating at random with different species in the clade, or do photobiont and mycobiont species associate preferentially? If preferential association occurs, to what extent are the phylogenies of the mycobiont and phycobiont lineages congruent? Few studies have directly addressed this question. It has generally been concluded that, since apparently identical photobionts are found associated with widely different mycobionts, then the mycobionts must similarly have little specificity for the phycobiont.

Available evidence, however, suggests that symbiont fidelity may be more common than previously assumed. Freidl (1987) reported host-switching in Diploschistes musorum which initially obtains its phycobiont, Trebouxia irregularis, through parasitizing squamules of Cladonia sp., but when the thallus is mature it is found to contain the phycobiont, Trebouxia showmanii, perhaps captured from soredia of other lichens, though evidence for the source of the phycobiont in mature thalli was not obtained. Bubrick and Galun (1980) and Bubrick et al. (1985) studied a phycobiont binding protein in Xanthoriaparietina that binds preferentially to one strain of phycobiont, suggesting a physiological mechanism for specificity. Friedl (1990?), studied phycobiont specificity in Parmelia and found that in nine species phycobiont isolates from multiple thalli revealed a single phycobiont associating with the mycobiont. In six species of Parmelia studied more than one phycobiont was found among multiple isolates, but in each case one of the phycobionts occurred in a majority of thalli sampled. The conclusion phycobiont specificity may have a strong phylogenetic component has recently gained support from a comparative study of nuclear rDNA ITS sequences obtained from Trebouxia isolated from Cladonia sp. Piercey-Normore and Depriest (1999) found high sequence similarity among Trebouxia isolates from several species of Cladonia representing three continents. The rDNA sequences of phycobiont isolates from geographically remote collections of Cladonia matched the sequence of T. erici isolated from Cladonia cristatella. Their finding suggests that closely related fungal lineages may prefer a single phycobiont genotype.

Beck et al. (1998) studied phycobiont specificity within a tightly knit corticolous lichen community using both light microscopy of cultured isolates and rDNA ITS sequence comparisons. They found that lichens without vegetative propagules occurring as pioneers on smooth bark were preferentially associated with T. arboricola. Two lichen species reproducing exclusively by vegetative propagules, Phaeophyscia orbicularis and Phycscia adscendens, were both associated with the phycobiont, T. impressa, but the isolates from those species were genetically distinct, suggesting possible codivergence in mycobiont and phycobiont lineages that reproduce as a symbiotic whole. The evidence they produced could not, however, unambiguously support the association of particular phycobiont lineages with particular reproductive modes.

There is also recent evidence for symbiont specificity at higher taxonomic levels. Rambold et al. (1998) reviewed literature on occurrence of phycobionts within the Lecanorales and concluded that at the ranks of suborder, family, and genus, mycobionts exhibit strong specificity for phycobionts. They suggest that restriction of Dictychloropsis and Coccomyxa to the families Biatoraceae, Megalosporaceae, and Peltigeraceae is consistent with their basal position in the clade. Other, non-basal families within Lecanorales are preferentially associated with the genera Asterochloris and Trebouxia. Asterochloris is found most often associated with members of the Cladoniineae, whereas Trebouxia is largely restricted to the Lecanoriineae.

Aside from these few recent empirical studies, the question of symbiont fidelity has not been widely studied. Morphological simplicity of green algal symbionts, primarily small coccoid species, discourages recognition of genetically distinct lineages, and the taxonomy of phycobionts is consequently less well developed than mycobiont taxonomy (Tschermak-Woess, 1988). Among algae that are virtually restricted to lichen thalli Trebouxia and Pseudotrebouxia, which occur as the primary phycobiont in 50-70% of known lichen species (Ahmadjian, 1982), have been most closely studied. Meticulous cultural studies and light microscopy are required to discern morphological characters useful in taxonomy of these plants (Ahmadjian, 1960; Archibald, 1975; Hildreth & Ahmadjian, 1981; Tschermak-Woess, 1989), and numerous species in Trebouxia and Pseudotrebouxia have been described using these methods.

The efficacy of using morphological characters to delimit species in these taxa has, however, been called into question. Hildreth and Ahmadjian (1981) isolated apparently identical strains of Trebouxia and Pseudotrebouxia from distantly related lichen thalli and concluded that phycobiont specificity for mycobionts is generally low. They also found high levels of variability in morphological characters within species, and suggested that some morphological criteria may be too restrictive in delimiting species. Even the morphological distinctiveness of these long-standing genera has been shown unreliable. Based on ultrastructural studies (Melkonian and Peveling, 1988), and more recently, on DNA sequence data (Friedl and Rokitta, 1997), it now appears that Trebouxia and Pseudotrebouxia are more properly considered as a single linage. Species presently assigned to Myrmecia have also been shown to be nested within the Trebouxia / Pseudotrebouxia clade (Friedl, 1995; Friedl and Rokitta, 1997).
 
 

LITERATURE CITED

Ahmadjian, V. 1993. The lichen photobiont - what can it tell us about lichen systematics? Bryologist 96: 310-313

Ahmadjian, V. 1988. The lichen alga Trebouxia: does it occur free-living? Pl. Syst. Evol. 158: 243-247.

Ahmadjian, V. 1960. Some new and interesting species of Trebouxia, a genus of lichenized algae. Amer. J. Bot. 47: 677-683.

Archibald, P. A., 1975. Trebouxia de Pulmaly (Chlorophyceae, Chlorococcales) and Pseudotrebouxia gen. Nov. (Chlorophyceae, Chlorosarcinales). Phycologia 14: 125-137.

Beck, A., T. Friedl, G. Rambold, 1998. Selectivity of photobiont choice in a defined lichen community: inferences from cultural and molecular studies. New Phytol. 139: 709-720.

Friedl, T. 1996. Evolution of the polyphyletic genus Pleurastrum (Chlorophyta): inferences from nuclear-encoded robosomal DNA equences and motile cell ultrastructure. Phycologia 35: 456-469.

Friedl, T. 1995. Inferring taxonomic positions and testing genus level assignments in coccoid green lichen algae: a phylogenetic analysis of 18S ribosomal RNA sequences from Dictyochloropsis reticulata and from members of the genus Myrmecia (Chlorophyta, Trebouxiophyceae Cl. Nov.). J. Phycol. 31: 632-639.

Friedl, T., C. Rokitta, 1997. Species relationships in the lichen alga Trebouxia (Chlorophyta, Trebouxiophyceae): molecular phylogenetic analyses of nuclear-encoded large subunit rRNA gene sequences. Symbiosis 23: 125-148.

Friedl, T., C. Zeltner, 1994. Assessing the relationships of some coccoid green lichen algae and the Microthamniales (Chlorophyta) with 18S ribosomal RNA gene sequence comparisons. J. Phycol. 30: 500-506.

Gupta, M., Y.-S. Chyi, J. Romero-Severson, J. L. Owen, 1994. Amplification of DNA markers from evolutionarily diverse genomes using single primers of simple-sequence repeats. Theo. Appl. Genet. 89: 998-1006.

Hildreth, K. C., V. Ahmadjian, 1981. A study of Trebouxia and Pseudotrebouxia isolates from different lichens. Lichenologist 13: 65-86.

Honegger, R. 1996. Mycobionts. In T. H. Nash [ed.] Lichen Biology, 24-36, Cambridge University Press.

Llano, G. A., 1950. A monograph of the lichen family Umbilicariaceae in the Western Hemisphere. Ph.D. thesis. Office of Naval Research, Navxos P-831. 281 pp.

Rambold, G., T. Friedl, A. Beck, 1998. Photobionts in lichens: possible indicators of phylogenetic relationships? Bryologist 101: 392-397.

Slocum, R. D., V. Ahmadjian, K. C. Hildreth, 1980. Zoosporogenesis in Trebouxia gelatinosa: ultrastructure potential for zoospore release and implications for the lichen association. Lichenologist 12: 173-187.

Stenroos, S. K., P. T. DePriest, 1998. SSU rDNA phylogeny of cladoniiform lichens. Amer. J. Bot. 85: 1548-1559.

Tschermak-Woess, E. 1989. Developmental studies in trebouxioid algae and taxonomical consequences. Pl. Syst. Evol. 164: 161-195.
 
 

This site was last updated on 31 March 2000.
Copyright © 2000 Steven L. Jessup, Southern Oregon University.