Overview of 75 years of Smittium research, establishing a new genus for Smittium culisetae, and prospects for future revisions of the ‘Smittium’ clade¹

1 This paper is dedicated to Dr Marvin Williams and his former students for their contributions to Smittium and other Harpellales and also to a former student of both Drs Williams and Lichtwardt, the late Dr Roger Grigg, whose isozyme studies, among others, have helped us unravel some of these stories.

Abstract

The Harpellales includes 38 genera of endosymbiotic microfungi associated with various Arthropoda. Smittium, the second genus to be described, is now also the most species rich of the order. Species of Smittium inhabit the digestive tracts of larval aquatic insects, especially lower Diptera, worldwide. During the 75 y since the type, Smittium arvernense, was described a number of advances in our understanding of the gut fungi have unfolded, in whole or in part, with Smittium as a model for the fungal trichomycetes. This in part relates to the high number of successful isolation attempts, with about 40% of known species having been cultured, a total number that far exceeds any other genus of gut fungus. Many isolates of Smittium have been used in laboratory studies for ultrastructural, physiological, host feeding, serological, as well as isozyme, and now ongoing molecular systematic studies. Molecular studies have shown that Smittium is polyphyletic but with consistent separation of Smittium culisetae, one of the most common and widespread species, from the remainder of Smittium. A brief overview of Smittium research is provided. Zygospore and trichospore morphology and molecular evidence (immunological, isozyme, DNA sequences and phyiogenetic analyses) are used to establish Zancudomyces and to accommodate Smittium culisetae. For the latter evidence, we include the first two-gene phylogenetic analysis, using combined 18S and 28S rRNA gene sequence data to show a cluster of Zancudomyces culisetae separate from Smittium. As the broadest taxon sampling of Smittium to date, this also serves a molecular systematic update toward revisionary syntheses of this and other Harpellales taxa.

Key words:

• Diptera
• early-diverging fungi
• Insecta
• Kickxellomycotina
• Symbiosis
• Zygomycota

Acknowledgments

Financial support from NSF REVSYS Award DEB-0918182 (to MMW) and DEB-0918169 (to RWL) are gratefully acknowledged for this and ongoing studies toward a molecular-based reclassification of the Harpellales and Asellariales. MMW also received financial support for some of the earlier sequences from a Martin-Baker Award from the Mycological Society of America. We present this work also in memory of the earlier work in France, from Poisson through Manier, and because we recently celebrated the 75th anniversary of the establishment of Smittium. We are exceedingly grateful for samples, whether dissected or accessioned as isolates in our culture collection, from our colleagues and friends working in the field, particularly to Drs CE Beard, MJ Cafaro, LC Ferrington Jr, CC López Lastra, G Mazzucchelli, WK Reeves, A Rizzo, D Strongman, T Sweeney, LG Valle, as well as R Willey, while also recognizing both longer term and ongoing collaborations with some of them as well. YW also thanks his committee, Drs James Smith and Steve Novak, for their helpful suggestions with project design, progress reviews and suggestions for this research. We also thank Jeremy Niece and staff at UWBC core facility for prompt support for sequencing reactions and data handling.

Notes

1 This paper is dedicated to Dr Marvin Williams and his former students for their contributions to Smittium and other Harpellales and also to a former student of both Drs Williams and Lichtwardt, the late Dr Roger Grigg, whose isozyme studies, among others, have helped us unravel some of these stories.