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a Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331; and b Institute of Marine Sciences, University of North Carolina at Chapel Hill, Morehead City, North Carolina 28557
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: ascomycetes • fungi • Halosphaeriales • large subunit (LSU) rDNA • marine • parsimony • small subunit (SSU) rDNA • systematics
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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As an extension of the Floridean hypothesis and a marine origin of the Ascomycota, marine ascomycetes are described as primary or secondary inhabitants of marine waters (Kohlmeyer, 1986). Primary marine species are hypothesized to be derived from ancestral lineages that originated in the marine environment. Secondary marine species represent the reintroduction of fungi into the marine environment and are hypothesized to share a more recent common ancestry with terrestrial lineages. Despite many studies and advances in molecular phylogenetics of fungi, the polarity of terrestrial–marine transitions within the Ascomycota has yet to be addressed. To gain insight into this evolutionary phenomenon, a molecular phylogenetic study that focused on the relationship of the Halosphaeriales to other groups of ascomycetes was initiated. The Halosphaeriales are the largest order of marine ascomycetes comprising over 130 marine (Kohlmeyer, 1986; Jones, 1995) and six freshwater species. Most species can be isolated in intertidal and subtidal zones where they degrade lignin and cellulose associated with plants and plant debris; a few are parasites of algae and marine animals. Fungi of the Halosphaeriales are hypothesized to be both of marine (Kohlmeyer, 1986) and terrestrial origin (Kirk, 1986), and because of these contradictory hypotheses, relationships among taxa in the Halosphaeriales are pivotal in understanding the evolution of marine and terrestrial ascomycetes.
Four morphological characters are pertinent to a discussion of the Halosphaeriales and warrant a brief discussion. These include (1) the sexual reproductive structure (ascocarp), (2) the central cavity (centrum) of the ascocarp, (3) sac-shaped ascospore producing structure (ascus), and (4) the meiospore (ascospore). Members of the Halosphaeriales possess flask-shaped ascocarps (Fig. 1A), or perithecia, which are characterized by an ostiole, i.e., a canal ending in a pore in the papilla or a neck. It is only after passing through the ostiolar canal that ascospores are eventually released into the environment. The central cavity or centrum (Fig. 1A) of the perithecium is the site of ascus and ascospore production and is initially filled with thin-walled pseudoparenchymatous polygonal cells (Fig. 1B). This pseudoparenchyma may develop into chains of sterile cells (catenophyses), which become interspersed among developing asci, or it may completely disappear in the mature perithecium. The asci (Fig. 1C) of most halosphaeriaceous fungi are clavate and are typically produced in a fascicle located at the basal region of the central cavity. In most species the ascus wall deliquesces prior to or at ascospore maturity, a phenomenon referred to as evanescent asci, resulting in ascospores that are not forcibly discharged. The ascospores are forced into the ostiolar canal of the perithecium by the production of additional asci and ascospores, and in intertidal species may be exuded in a droplet at the tip of the neck prior to being dispersed by water. The often uniquely appendaged or sheathed ascospores (Fig. 1D, E) are the hallmark of the Halosphaeriales (Jones, 1995). The ascospore wall is described as possessing two or three layers. The innermost layer is termed the mesosporium, the middle layer is the episporium, and the outermost layer, missing in a number of genera, is the exosporium (Jones, 1995). The ascospore appendages and sheaths are derived mainly from the epi- and/or the exosporium and are genus specific. The appendaged ascospores are interpreted as adaptations to the marine environment by increasing surface area for water dispersal and adherence to appropriate substrates. Most genera possess ascospores that are ellipsoidal to fusiform and are one-celled to several septate (Fig. 1D, E); however, a few genera (e.g., Lindra and Lulworthia) possess long filiform ascospores (Fig. 1F) that may or may not be septate according to species.
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The goal of this study was to test and refine phylogenetic hypotheses central to the Halosphaeriales. Specific hypotheses addressed were (1) the monophyly of the order, (2) supraordinal taxonomic affinities of the Halosphaeriales among the phylum Ascomycota, (3) the evolution of evanescent asci and ascospore appendages within the order, and (4) the polarity of marine–terrestrial transitions within the Ascomycota as it pertains to the Halosphaeriales. These questions were addressed using phylogenetic analyses of nucleotide sequences of the genes that code for the nuclear small (SSU rDNA) and large (LSU rDNA) ribosomal RNAs.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Sequences were added to a pre-existing database of homologous sequences from an alignment of terrestrial ascomycetes. The initial alignments were performed using the Pileup program of GCG (Wisconsin Package Version 8.0, Genetics Computer Group, Madison, Wisconsin) with default settings; alignments were then refined by direct examination using SeqApp (Gilbert, 1997). (The alignments are available on the Internet at <http://www.orst.edu/Dept/botany/mycology/> or from JWS upon request.) Maximum parsimony and weighted parsimony analyses of the SSU and LSU rDNA sequences were performed using PAUP 3.1.1 and PAUP* (Swofford, 1993, 1997). Weighted parsimony analyses were performed using a step matrix to weight nucleotide transformations based on the reciprocal of the observed transition:transversion ratio from the maximum parsimony analyses. Transition:transversion biases were calculated using MacClade 3.0 (Maddison and Maddison, 1992). Unambiguous gaps were included in the analyses, coded as a fifth state using the GAPMODE = NEWSTATE option, and given a weight of one for all possible transformations in weighted parsimony analyses. Due to the number of taxa, only heuristic searches were possible. Twenty-five heuristic replicate searches were performed employing branch-swapping with tree-bisection-reconnection (TBR) and random sequence addition with an initial random seed number of 1 999 999. Using the described heuristic search options, bootstrap values (Felsenstein, 1985) were calculated from 250 replications and decay indices (Bremer, 1988; Donoghue et al., 1992) were calculated for up to five steps.
Two sets of complementary analyses, which differed in the level of taxon sampling, were performed. The first set included maximum and weighted parsimony analyses of partial SSU rDNA sequences from 38 taxa from 15 orders of ascomycetes and three outgroup taxa of basidiomycetes (Fig. 2). This broad taxon sampling of the major groups within the Ascomycota was performed to test the close phylogenetic relationship of the Halosphaeriales to other perithecial ascomycetes. A second set of phylogenetic analyses, which focused on the perithecial ascomycetes, was performed on a combined data set of SSU and LSU sequences. Analyses included 15 isolates from the Halosphaeriales and 31 terrestrial perithecial ascomycetes and were performed without (Fig. 3) and with (Fig. 4) outgroup taxa to test for differences in ingroup topologies resulting from the inclusion of the outgroup. Because the Pezizales represented the only nonperithecial order of the Euascomycetes for which both SSU and LSU rDNA sequences were available, four pezizalean taxa were chosen as outgroup representatives. Separate step matrices were used to assign unique TN:TV weights to the SSU and LSU rDNA regions in the combined analyses using the "Set Character Type" menu option in PAUP 3.1.1.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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These initial SSU rDNA analyses, which included the halosphaeriaceous taxa Halosphaeria appendiculata Linder, Corollospora maritima Werderm., Lulworthia grandispora Meyers, and Lindra marinera Meyers, did confidently confirm the close phylogenetic relationship of the Halosphaeriales with perithecial ascomycetes, i.e., Diaporthales, Hypocreales, Microascales, Sordariales, and Xylariales (Fig. 2). This relationship was observed in both maximum and weighted parsimony analyses and received a bootstrap value and decay index of 100% and >5, respectively. Although the initial taxon sampling was small and was intended only to test a hypothesis regarding supraordinal relationships of the Halosphaeriales, it did not support the monophyly of the order. Of the four halosphaerialean taxa sampled, H. appendiculata and C. maritima were placed as a sister group to Microascus trigonosporus C.W. Emmons and B.O. Dodge, and L. marinera and L. grandispora formed a well-supported clade that was isolated among the perithecial ascomycetes (Fig. 2).
In the second set of analyses, combined analyses were performed on SSU and LSU rDNA sequences, which included 15 halosphaeriaceous taxa and 26 taxa from eight orders of terrestrial perithecial ascomycetes. Both maximum and weighted parsimony analyses were conducted without (Fig. 3) and with (Fig. 4) five outgroup taxa from the Pezizales. The SSU rDNA alignment corresponds to the region described above, included seven unambiguous single position indels, and contained 263 potential synapomorphies. Sequence alignments of the LSU rDNA included 590 nucleotide positions, which correspond to positions 68–735 in Saccharomyces cerevisiae (GBANM27607). Three regions proved problematic in alignments and resulted in 40 bp being excluded from the analyses because of the high degree of sequence alignment ambiguity. These regions consisted of indels that varied in length among the taxa surveyed and corresponded to nucleotides 127–137 of region A and nucleotides 501–506 and 532–541 of region B from the predicted LSU rRNA secondary structure of S. cerevisiae (Gutell and Fox, 1988). The remaining 550 LSU nucleotide positions contained five single position indels and four double-position indels and possessed 221 potential synapomorphies. The combined SSU and LSU rDNA dataset included 1609 nucleotide positions of which 484 (30.08%) were identified as potential synapomorphies.
Two most parsimonious trees of 1727 steps with CI and RI of 0.393 and 0.626, respectively, were inferred in a maximum parsimony analysis of only perithecial ascomycetes, i.e., no outgroup taxa were included. The only polytomy involved a monophyletic vs. a paraphyletic resolution of the Clavicipitaceae (Hypocreales). The observed TN:TV ratio was 1.4 and 1.7 for the SSU and LSU rDNA, respectively. A single most parsimonious tree was inferred in a second analysis in which transversions were weighted 1.4 and 1.7 times greater than transitions for the SSU and LSU rDNA regions of the data, respectively. The weighted tree contained all the same major groups as the maximum parsimony tree, however the Clavicipitaceae were resolved as monophyletic and several rearrangements existed within the halosphaeriaceous clade containing Ceriosporopsis halima Linder and Corollospora maritima (data not shown). This latter clade, although well supported within the Halosphaeriales, was itself not strongly supported by bootstrapping or decay indices. Because no topological differences existed among the major clades between the maximum parsimony trees and the weighted parsimony tree, an unrooted phylogram of the maximum parsimony tree with the monophyletic Clavicipitaceae is presented in Fig. 3. A single most parsimonious tree of 2167 steps with CI and RI of 0.389 and 0.630, respectively, was inferred in a maximum parsimony analysis of perithecial ascomycetes with outgroup taxa from the Pezizales included. Identical TN:TV ratios to the tenth decimal place were observed as in the no-outgroup analysis, and transversions were weighted more than transitions as described above. A single most parsimonious tree, which again only differed from the maximum parsimony analysis in rearrangements of taxa restricted to the Ceriosporopsis halima–Corollospora maritima clade (data not shown), was inferred in the weighted analysis. A phylogram of the maximum parsimony tree is presented in Fig. 4. This second set of analyses, which focused on an expanded taxon sampling of the Halosphaeriales and terrestrial perithecial ascomycetes, again inferred two separate clades of halosphaeriaceous fungi (Figs. 3, 4) and thus confirmed the polyphyly of the Halosphaeriales. The largest clade comprises 12 taxa from 11 genera and is a sister group to the Microascales. This clade represents the Halosphaeriales sensu stricto and consists of the type genus Halosphaeria as well as other typical halosphaeriaceous genera. The second clade of halosphaeriaceous taxa consists of the isolates sampled from the genera Lindra and Lulworthia. Although the Lindra/Lulworthia clade is isolated among the perithecial ascomycetes, i.e., it does not exhibit an especially close sister-group relationship to any of the other fungi sampled (Figs. 3, 4), it is a member of the larger monophyletic clade of perithecial fungi (Fig. 2).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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These data led us to ask whether the ancestral character states for the Microascales/Halosphaeriales clade and the more inclusive perithecial ascomycete clade are marine or terrestrial, i.e., did the terrestrial forms give rise to the Halosphaeriales or vice versa? Taxa were coded as marine or terrestrial and character state changes were mapped onto the most parsimonious tree using MacClade 3.0 (Fig. 5; Maddison and Maddison, 1992). The most parsimonious explanation is a terrestrial origin of the Halosphaeriales s.s., rather than a marine origin of the Microascaceae, Ceratocystis, and other closely related terrestrial, perithecial ascomycetes. Not only are the closest relatives to the Halosphaeriales s.s. terrestrial fungi, but they are intimately associated with arthropods and rely on them for ascospore dispersal (Skou, 1973; Crowson, 1984; Malloch and Blackwell, 1992). Therefore, the terrestrial to marine adaptation in the common ancestor of the Halosphaeriales s.s. may have also been accompanied by the loss of arthropod dispersal of ascospores.
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The phylogenetic integration of marine and terrestrial forms provides insight into the evolution of asci and ascospores among terrestrial and marine ascomycetes that could not be achieved by separate studies of either. The plasticity of ascus morphology and dehiscence is consistent with a character that is strongly affected by selection pressures (Cain, 1972). It has been argued that evanescent asci have evolved repeatedly among terrestrial fungi, and that the nonhomology of evanescent asci among some different groups of fungi represents convergent evolution for arthropod-dispersal of ascospores (Malloch and Blackwell, 1992; Blackwell, 1994). While these data strongly support that hypothesis (Figs. 3, 4), the evanescent asci of ecologically disparate fungi, i.e., the terrestrial Microascales and the marine Halosphaeriales s.s., are homologous character states.
Additionally, the data suggest that reversals from evanescent asci to persistent asci with forcibly discharged ascospores may have also occurred. The majority of species in the Halosphaeriales s.s. have evanescent asci, however a few taxa including Halosarpheia fibrosa Kohlm. and E. Kohlm., Lignincola laevis Höhnk, and Aniptodera juncicola Volkm.-Kohlm. and Kohlm. possess persistent asci. While only a single gain is needed to explain the distribution of evanescent asci among Ceratocystis, the Microascaceae, and Halosphaeriales s.s., the phylogenetic hypothesis presented here requires three reversals from evanescent to persistent asci within the Halosphaeriales s.s. (Fig. 4). The multiple origins of evanescent asci have received recent attention in the context of molecular systematics of ascomycetes (Berbee and Taylor, 1992; Blackwell, 1994; Spatafora and Blackwell, 1994). However, the potential for reversals from evanescent to persistent asci has not been addressed. Evanescent asci have been viewed as a loss of persistent asci. An alternative interpretation, which is consistent with the reversal to persistent asci, is that the evanescent character state represents an evolutionary gain. That is, those taxa that possess evanescent asci may actually possess unique cellular or enzymatic attributes that maintain the character state of evanescent asci, and that the loss of this capability results in the reversal to persistent asci. Alternatively, the possession of persistent asci by relatively few halosphaeriaceous taxa may represent the retention of a primitive character state rather than a reversal to a primitive state (e.g., Aniptodera juncicola Volkm.-Kohlm. and Kohlm.). These two evolutionary scenarios are both in agreement in that persistent asci are primitive, but they differ in the implicit interpretation concerning the derivation of the evanescent character state. Unfortunately, little is known about the molecular genetics and physiology of evanescent ascus production, and whether there might be fundamentally different, i.e., nonhomologous, biochemical mechanisms functioning in different groups of fungi.
Analogous to the homoplasy in ascus dehiscence is the evolution of ascospore appendages. Although both groups of Halosphaeriales in Figs. 2–4
contain taxa with ascospores described as producing appendages (Jones and Moss, 1987), those of Lindra and Lulworthia are strikingly different from the appendages of the Halosphaeriales s.s. (Fig. 1D–F). The ascospores of Lulworthia may be better described as possessing apical chambers that are filled with mucus, which is released to facilitate attachment of ascospores (Jones, 1995). The ascospores of Lindra do not possess such structures. The rejection of the homology between the ascospore apical chambers of Lulworthia and the ascospore appendages of the Halosphaeriales s.s. is consistent with the phylogenetic hypothesis proposed here (Fig. 4). In addition, just as reversals in ascus dehiscence were detected within the Halosphaeriales s.s., so was the loss in the production of ascospore appendages. While most taxa within the Halosphaeriales s.s. form ascospore appendages, a minority of halosphaerialean taxa do not (e.g., Lignincola laevis); furthermore, the production of ascospore appendages is not restricted to marine fungi. They are produced by many terrestrial, especially coprophilous, fungi (e.g., Podospora spp. of the Sordariales) and are generally assumed to increase spore surface area to facilitate ascospore attachment and dispersal via a variety of dispersal mechanisms. The data presented here suggest that the ability to produce ascospore appendages was present in the common ancestor of the Halosphaeriales s.s. and that those taxa that lack ascospore appendages have lost the ability to produce such structures (Fig. 4).
Another major aspect in the evolution of marine ascomycetes that can be addressed with these data is the phylogenetic connection of sexual and asexual taxa within the Halosphaeriales s.s. Ascomycete life cycles are often characterized by sexual (teleomorphic) and asexual (anamorphic) states (reviewed in Reynolds and Taylor, 1993). Marine ascomycetes exhibit considerable morphological variation among anamorphs of closely related and morphologically similar teleomorphs (Shearer, 1986; Nakagiri and Tubaki, 1987). For this reason, understanding the evolution of anamorphs among marine ascomycetes and establishing definitive links between teleomorphs and anamorphs is often difficult. The striking resemblance of sclerocarps (asexual reproductive structures) of Varicosporina ramulosa Meyers and Kohlm. with ascocarps (sexual reproduction structures) of Corollospora spp. led to the hypothesis that V. ramulosa is an ascomycete that has lost its ability to reproduce sexually (Kohlmeyer and Charles, 1981; Nakagiri, 1986). The data presented here support a close relationship between them and illuminate the need for the inclusion of Varicosporina spp. in systematic studies of Corollospora Werderm. and for increased taxon sampling of anamorphs with no known teleomorphs in molecular phylogenetics of marine ascomycetes.
The multiple origins of both the marine habit and evanescent asci provide valuable observations for refining evolutionary hypotheses among the perithecial ascomycetes. These results are consistent with the hypothesis of the common ancestor of perithecial ascomycetes being a terrestrial fungus with persistent asci and forcibly discharged ascospores. Evanescent asci were derived several times in terrestrial ecosystems in conjunction with and in the absence of arthropod dispersal of ascospores. At least one lineage of terrestrial, arthropod-associated perithecial ascomycetes with evanescent asci gave rise to fungi that adapted to the marine environment, i.e., the Halosphaeriales s.s. Also, three reversals from evanescent to persistent asci as well as gains and losses of ascospore appendages have occurred within the Halosphaeriales s.s. The level of homoplasy present in the character states of asci and ascospores among the taxa sampled exemplifies the challenge in understanding the evolution of fungal morphology. Furthermore, this study highlights the role molecular phylogenetics can play in providing an independent assessment of morphological character state homology. Future work should focus on the continued integration of marine, terrestrial, and arthropod-associated fungi as they pertain to the evolution of terrestrial–marine transitions within the Ascomycota.
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FOOTNOTES |
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4 Author for correspondence (email:spatafoj{at}bcc.orst.edu
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J. Campbell and C. A. Shearer Annulusmagnus and Ascitendus, two new genera in the Annulatascaceae Mycologia, July 1, 2004; 96(4): 822 - 833. [Abstract] [Full Text] [PDF]
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J. Campbell, J. L. Anderson, and C. A. Shearer Systematics of Halosarpheia based on morphological and molecular data Mycologia, May 1, 2003; 95(3): 530 - 552. [Abstract] [Full Text] [PDF]
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 K. J. Peterson, B. Waggoner, and J. W. Hagadorn A Fungal Analog for Newfoundland Ediacaran Fossils? Integr. Comp. Biol., February 1, 2003; 43(1): 127 - 136. [Abstract] [Full Text] [PDF]
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J. Campbell, C. A. Shearer, J. L. Crane, and P. M. Fallah A reassessment of two freshwater ascomycetes, Ceriospora caudae-suis and Submersisphaeria aquatica Mycologia, January 1, 2003; 95(1): 41 - 53. [Abstract] [Full Text] [PDF]
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E. C. Y. Liew, A. Aptroot, and K. D. Hyde An evaluation of the monophyly of Massarina based on ribosomal DNA sequences Mycologia, September 1, 2002; 94(5): 803 - 813. [Abstract] [Full Text] [PDF]
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