Mary Berbee

Professor

Research Classification

Evolution and Phylogenesis
Microorganisms
Taxonomy and Systematics

Research Interests

systematics
molecular phylogenetics
fungi
mycology

Relevant Degree Programs

 

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Master's students
Doctoral students
2019
I support experiential learning experiences, such as internships and work placements, for my graduate students and Postdocs.
I am open to hosting Visiting International Research Students (non-degree, up to 12 months).

Graduate Student Supervision

Doctoral Student Supervision (Jan 2008 - May 2019)
Evaluating morphology and geographic range extent of genetically delimited species of mushrooms (2018)

Species delimitation directly affects interpretation of evolution and biogeography. Following speciation, independently evolving lineages are expected to fix different characters that eventually distinguish them from their closest relatives. However, rates of fixation vary. I delimited species in the mushroom genus Russula based on the fungal nuclear internal transcribed spacer 2 (ITS2) DNA barcode region. I sampled 713 ITS2 sequences of American Pacific Northwest specimens collected by Seattle architect Benjamin Woo (1923-2008). I compared the morphology within and among DNA-delimited species, according to morphological character state data that Woo had recorded for each of specimen. To Woo's data, I added spore measurements for 23 species. The characters in Russula varied within and overlapped between my delimited species. My multivariate analysis showed that the centroids of morphological characters usually differed significantly between pairs of genetically defined species, indicating evolutionary divergence at the level of morphology. However, because of the variation among and within conspecific collections, morphological characters only correctly predicted the identity of ~50% of the individual specimens. Of the delimited species, nine had been collected ten or more times each and were, based on morphology and sequence analysis, undescribed and restricted to North America. I describe the nine as new species, reporting their character variation. I used data from public databases to ask how frequently geographical ranges are intercontinental as opposed to intracontinental among mushroom-forming species. I calculated the ‘range extent’ (maximum geographical distance) recorded for 2324 species world-wide and 341 species from the Pacific Northwest, representing 12 genera. The ranges of most species extended only to ~2000 km (shorter distances than a continent). By permutation of the data, I showed that this pattern vanished if geographical coordinates were randomized with respect to species suggesting the pattern I found in the data was not due to random sampling. More sampling would be needed to resolve whether the pattern arose from sampling bias or a high frequency of regional endemism. However, because it reflects a common pattern seen in the best sampled fungi and in narrower studies of genera and families, I hypothesize that regional endemism is the general pattern in well-studied genera and more generally fungal biogeography.

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How the Fungi got into shape : cellular organization and morphogenetic gene evolution in phylum Chytridiomycota reveals mechanisms underlying the evolution of fungal body diversity (2018)

With their threadlike hyphal cells, fungi can invade the surface of a cheese, secreting digestive enzymes and soaking up the spoils. Although most fungi feed with hyphae, phylum Chytridiomycota produces various alternative cell shapes. Here I address three hypotheses regarding the evolution of cell shape. Firstly, Fungi inherited core genes for cellular morphogenesis from their most recent common ancestor and diversification of these genes through evolutionary time potentially contributed to morphological novelty. My phylogenomic surveys revealed duplications in seven families of actin-binding proteins predating the radiation of fungal phyla. Synthesizing previous studies of the function, localization and evolutionary history of septin, myosin, and actin-binding proteins in yeasts and hyphal fungi enabled me to further hypothesize their roles during development in Chytridiomycota. Since Chytridiomycota diverged from moulds and mushrooms, each group evolved unique mechanisms for constructing different cell shapes using a shared ancestral molecular toolkit.Hyphal growth and septation require actin. My second hypothesis was that actin, a major cytoskeletal component, is also involved in morphogenesis in Chytridiomycota. Using fluorescence microscopy, I documented rhodamine phalloidin-stained actin cables, patches, sheets and perinuclear shells through development in Chytriomyces hyalinus. I disrupted the actin cytoskeleton with the chemical inhibitor latrunculin B. Observing actin patches concentrated at rhizoid tips and at cytoplasmic cleavage planes, and finding that actin integrity was essential for rhizoid proliferation in C. hyalinus both support a conserved role for actin in polarized growth and cytokinesis.Thirdly, I hypothesized that sustained tip growth and nuclear migration underlie the convergent evolution of hyphae and hypha-like growth forms. Chytriomyces hyalinus shows determinate growth that ceases once a zoosporangium matures. Phylogenies indicate that filamentous species in Chytridiomycota with indeterminate growth arose independently from ancestors with a determinate growth mode. I determined that actin organization and nuclear migration patterns in each species differed from one another and from hyphae, most likely as a result of their independent origins. In combination, phylogenetic analyses, molecular genetics, and microscopy are tearing away the curtains of time that mask the ever-changing molecular machinery that gave rise to an astounding diversity of form and function in modern fungi.

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New ichthyosporean protists and their biology as inferred from molecular genetic and light and electron microscopic study (2010)

Precipitated by unexpected discoveries, this thesis is dedicated to the study of the biology of ichthyosporeans. While searching for undiscovered opisthokonts living osmotrophically in marine invertebrate digestive tracts, I established 177 cultures of ichthyosporeans. Ichthyosporeans are one of six understudied unicellular lineages related to the multicellular animals and fungi. Ichthyosporeans are comprised of approximately 30 genera but, prior to this thesis, only four genera had been cultivated. I identified and described three new genera and six species using microscopy and molecular phylogenetic techniques. Two, which I named Abeoforma whisleri and Pirum gemmata, were most closely related to divergent clone sequences and had no known relatives. My other four species, each isolated between eight and 126 times, were related to single isolates Sphaeroforma arctica and Pseudoperkisus tapetis, also found in marine invertebrates. I described one as the new genus and species Creolimax fragrantissima because of its amoeboid reproductive and dispersal stage and fragrance. The other three species were closely related and morphologically indistinguishable. To delimit species, I sequenced three loci from multiple isolates and applied a genealogical concordance species concept. Once delimited, I was able to describe variations in life cycle, morphology and a possible difference in host preference. Rather than adapt cytological techniques to describe the life cycle of S. tapetis, the most abundant species, I used population genetics to work in reverse. Absence of heterozygotes provided evidence for haploidy. Phylogenetic incongruence and a lack of support for linkage between two loci signified a history of recombination consistent with a sexual cycle. I described the ultrastructure of five species using high-pressure frozen cells from healthy, luxuriantly growing cultures. The quality of preservation allowed me to describe features that were new to ichthyosporeans, such as, spindle pole bodies and tubular extensions of the cell that penetrated the cell wall. These features were found in both clades and may have been present in the ancestral ichthyosporean. By combining genetic evidence for sex, observations of asexual reproduction in culture and collection frequencies I proposed a life cycle involving infrequent recombination within a predominantly asexual organism that infected invertebrate hosts indiscriminately via asexual endospores.

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Master's Student Supervision (2010 - 2018)
Taxonomy and phylogeny of mitosporic Capnodiales and description of a new sooty mold species, Fumiglobus pieridicola, from British Columbia, Canada. (2013)

Sooty molds from Capnodiaceae are epiphyllous saprotrophs that are often associated with sap-sucking insects. The honeydew exuded by these insects serves as the nutritive substrate for the molds. Through this study I identify an unknown sooty mold on Japanese andromeda, Pieris japonica, from northwestern North America. Morphological analysis of the pycnidial state suggested the fungus is a Fumiglobus species, but with substantial differences from the previously reported species from the genus. In this thesis, I illustrate and describe the epiphyllous mold as Fumiglobus pieridicola. I also provide partial 18S and 28S ribosomal gene sequence data for F. pieridicola. These are the first sequences determined for any species in the genus. Using my sequence dataset, I show that the genus Fumiglobus is within Capnodiaceae with considerable bootstrap support. I also furnish new sequences for the type species of the mitosporic genus Conidiocarpus, also in Capnodiaceae. I confirm that Conidiocarpus is the anamorph of Phragmocapnias. Following the rules of nomenclatural priority, I synonymize Phragmocapnias species under Conidiocarpus. Using ancestral character state reconstruction for Capnodiales, I find a high probability that the ancestor for Capnodiaceae was pycnidial. My analyses contribute to an improved molecular and morphological definition of Capnodiaceae.

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A different shade of hypha : cytological and molecular phylogenetic evidence for the independent rise of the hyphal habit in the class Monoblepharidomycetes (Chytridiomycota) (2011)

Once the ancestors of fungi stopped moving and instead started reaching out with hyphae, their filamentous growth made possible new variety in form and habitat. Hyphae mediated substrate colonization, absorptive nutrition, mating and reproduction. Although shared across most familiar terrestrial fungal lineages, little was known about where hyphae evolved in early fungi. In chapter one, I review the phylogenetic origins of hyphae and current understanding of the cytology of hyphal tips. Better understanding of fungal phylogeny and hyphal growth near the base of the fungal tree was needed. In Chapter 2, I investigated the phylogeny and cytology in the Class Monoblepharidomycetes (Chytridiomycota), a group of deeply diverging, zoosporic fungi, encompassing a range of body types. Species can be either crescent or rod-shaped unicells or sprawling hyphal growths. I inferred a phylogeny of the fungi based on 28S ribosomal DNA sequence data using maximum likelihood (ML) and Bayesian inference methods. I recovered the monophyly of modern fungal phyla and the topology was comparable to the most taxonomically diverse and gene–rich phylogeny of the fungi to date. I used likelihood methods to trace the origins of hyphae on my likelihood tree, concluding that hyphae arose independently in the Monoblepharidomycetes and at least three other times in the fungi. Next, I searched for evidence of convergent evolution in the cellular organization of hyphal Monoblepharidomycetes using fluorescence and transmission electron microscopy. I showed that the hyphae of Monoblepharidomycetes have a novel form with an unusual microtubule cytoskeleton and without a typical fungal Spitzenkörper. This constitutes the first report on the cytology of hyphae from the Chytridiomycota. In Chapter 3, I discuss the significance of my research and possible future directions including cytological experiments on the Monoblepharidomycetes cytoskeleton.

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Forest stand type and ectomycorrhizal fungal communities of western hemlock on northern Vancouver Island, Canada (2010)

This thesis explores the diversity and phylogenetic structure of the ectomycorrhizal fungal community of western hemlock from five forest types on northern Vancouver Island. Chapter One reviews methods and provides background for studies of ectomycorrhizal fungal communities. In Chapter Two, I describe the results of a new correlative study using recently developed measures of phylogenetic diversity as well as standard measures of diversity and of fungal species composition to relate ectomycorrhizal fungal species to productivity of hemlock trees. I sampled ectomycorrhizal root tips of western hemlock from northern Vancouver Island and amplified, cloned and sequenced the fungal DNA from root extracts. In my analyses, I combined new data from plots of mature western hemlock-amabilis fir stands on Hemlock-Amabilis fir (HA) sites, and from plots of old-growth western red cedar-western hemlock stands on Cedar-Hemlock (CH) sites, with data previously gathered from plots of 24-year-old regenerating hemlock on CH sites. I detected 147 operational taxonomic units among 1435 fungal clone sequences. Phylogenetic diversity indices showed that mature hemlock stands on HA sites had significantly higher ectomycorrhizal fungal diversity than regenerating hemlock stands on CH sites. In an analysis of beta diversity, I found that the species composition of the 24-year-old stands was more similar to the composition of old-growth stands on CH sites than to the species composition of mature stands on HA sites. Fungal species composition was strongly correlated with foliar nitrogen concentration. My phylogenetic analyses of net relatedness of species from forests of different types provided some of the first insights into how ectomycorrhizal fungal communities are structured. I found phylogenetic clustering in the plots of 24-year-old regenerating hemlock stands that contrasted with a pattern of phylogenetic evenness in the plots of mature and old-growth stands. A possible explanation for the difference between the patterns is that the regenerating hemlock stands were selecting for related, r-adapted fungi with similar traits while the older stands had more complex environments and selected for divergent fungi with varied traits. Finally, in Chapter Three I discuss some limitations and strengths of my research study, incorporating ideas on future research and implications.

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