skip to main content


Title: The Early Terrestrial Fungal Lineage of Conidiobolus—Transition from Saprotroph to Parasitic Lifestyle
Fungi of the Conidiobolus group belong to the family Ancylistaceae (Entomophthorales, Entomophthoromycotina, Zoopagomycota) and include over 70 predominantly saprotrophic species in four similar and closely related genera, that were separated phylogenetically recently. Entomopathogenic fungi of the genus Batkoa are very close morphologically to the Conidiobolus species. Their thalli share similar morphology, and they produce ballistic conidia like closely related entomopathogenic Entomophthoraceae. Ballistic conidia are traditionally considered as an efficient tool in the pathogenic process and an important adaptation to the parasitic lifestyle. Our study aims to reconstruct the phylogeny of this fungal group using molecular and genomic data, ancestral lifestyle and morphological features of the conidiobolus-like group and the direction of their evolution. Based on phylogenetic analysis, some species previously in the family Conidiobolaceae are placed in the new families Capillidiaceae and Neoconidiobolaceae, which each include one genus, and the Conidiobolaceae now includes three genera. Intermediate between the conidiobolus-like groups and Entomophthoraceae, species in the distinct Batkoa clade now belong in the family Batkoaceae. Parasitism evolved several times in the Conidiobolus group and Ancestral State Reconstruction suggests that the evolution of ballistic conidia preceded the evolution of the parasitic lifestyle.  more » « less
Award ID(s):
1441715
NSF-PAR ID:
10392803
Author(s) / Creator(s):
; ; ; ; ; ; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Journal of Fungi
Volume:
8
Issue:
8
ISSN:
2309-608X
Page Range / eLocation ID:
789
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Wilson, Richard A. (Ed.)

    Trichodermais a cosmopolitan genus with diverse lifestyles and nutritional modes, including mycotrophy, saprophytism, and endophytism. Previous research has reported greater metabolic gene repertoires in endophytic fungal species compared to closely-related non-endophytes. However, the extent of this ecological trend and its underlying mechanisms are unclear. Some endophytic fungi may also be mycotrophs and have one or more mycoparasitism mechanisms. Mycotrophic endophytes are prominent in certain genera likeTrichoderma, therefore, the mechanisms that enable these fungi to colonize both living plants and fungi may be the result of expanded metabolic gene repertoires. Our objective was to determine what, if any, genomic features are overrepresented in endophytic fungi genomes in order to undercover the genomic underpinning of the fungal endophytic lifestyle. Here we compared metabolic gene cluster and mycoparasitism gene diversity across a dataset of thirty-eightTrichodermagenomes representing the full breadth of environmentalTrichoderma’s diverse lifestyles and nutritional modes. We generated four newTrichoderma endophyticumgenomes to improve the sampling of endophytic isolates from this genus. As predicted, endophyticTrichodermagenomes contained, on average, more total biosynthetic and degradative gene clusters than non-endophytic isolates, suggesting that the ability to create/modify a diversity of metabolites potential is beneficial or necessary to the endophytic fungi. Still, once the phylogenetic signal was taken in consideration, no particular class of metabolic gene cluster was independently associated with theTrichodermaendophytic lifestyle. Several mycoparasitism genes, but no chitinase genes, were associated with endophyticTrichodermagenomes. Most genomic differences betweenTrichodermalifestyles and nutritional modes are difficult to disentangle from phylogenetic divergences among species, suggesting thatTrichodermagenomes maybe particularly well-equipped for lifestyle plasticity. We also consider the role of endophytism in diversifying secondary metabolism after identifying the horizontal transfer of the ergot alkaloid gene cluster toTrichoderma.

     
    more » « less
  2. Abstract

    The frenulum is a wing coupling structure that is found on the wings of most families of Lepidoptera. It is a single bristle or set of bristles that originate from the base of the hindwing that often interlocks with the forewing during flight. This wing coupling mechanism is thought to have been a major evolutionary innovation that allowed for enhanced flight in Lepidoptera. The sack‐bearer moths (Mimallonidae) are unusual among Lepidoptera in that not all species within the family have a frenulum. We test the hypothesis that the frenulum is not necessary and is therefore lost in mimallonids that have longer male forewings, because such wings are perhaps better suited to be coupled by other means. To understand the evolution of the frenulum, we inferred the most taxonomically and genetically sampled anchored hybrid enrichment‐based phylogeny of Mimallonidae, including 604 loci from all 41 genera and from 120 species, covering about 40% of the described species in the family. The maximum likelihood tree robustly supports major relationships within the family, and ancestral state reconstruction clearly recovers the frenulum as the plesiomorphic condition in Mimallonidae. Our results show that the frenulum is more often observed in species that have shorter, rather than longer, male forewings. The frenulum has historically been used as an important character for intrafamilial classification in Mimallonidae, but our results conclusively show that this character system is more variable than previously thought. Based on our results, we erect two new subfamilies, Roelofinae St Laurent & Kawahara,subfam.n.and Meneviinae St Laurent, Herbin, & Kawahara,subfam.n., for four genera previously consideredincertae sedis.In the predominantly frenulum‐lacking clade Cicinninae, we describe a new genus,CerradocinnusSt Laurent, Mielke, & Kawahara,gen.n., and the genusGonogrammastat. rev.is revalidated to include many species previously placed inCicinnussensu lato. With these changes,Cicinnuscan now be considered monophyletic. Thirty‐three species are transferred toGonogrammafromCicinnussensu lato.

    This published work has been registered on Zoobank,http://zoobank.org/urn:lsid:zoobank.org:pub:E33100E1‐DA6A‐4814‐A312‐36CBAA168B8B.

     
    more » « less
  3. Abstract

    Fungus‐farming ants (Hymenoptera: Formicidae) have become model systems for exploring questions regarding the evolution of symbiosis. However, robust phylogenetic studies of both the ant agriculturalists and their fungal cultivars are necessary for addressing whether or not observed ant–fungus associations are the result of coevolution and, if so, whether that coevolution has been strict or diffuse. Here we focus on the evolutionary relationships of the species within the ant genusMyrmicocryptaand of their fungal cultivars. The fungus‐farming ant genusMyrmicocryptawas created by Fr. Smith in 1860 based on a single alate queen. Since then, 31 species and subspecies have been described. Until now, the genus has not received any taxonomic treatment and the relationships of the species within the genus have not been tested. Our molecular analyses, using ∼40 putative species and six protein‐coding (nuclear and mitochondrial) gene fragments, recoverMyrmicocryptaas monophyletic and as the sister group of the genusMycocepurusForel. The speciesM. tuberculataWeber is recovered as the sister to the rest ofMyrmicocrypta. The time‐calibrated phylogeny recovers the age of stem groupMyrmicocryptaplus its sister group as 45 Ma, whereas the inferred age for the crown groupMyrmicocryptais recovered as 27 Ma. Ancestral character‐state analyses suggest that the ancestor ofMyrmicocryptahad scale‐like or squamate hairs and that, although such hairs were once considered diagnostic for the genus, the alternative state of erect simple hairs has evolved at least seven independent times. Ancestral‐state analyses of observed fungal cultivar associations suggest that the most recent common ancestor ofMyrmicocryptacultivated clade 2 fungal species and that switches to clade 1 fungi have occurred at least five times. It is our hope that these results will encourage additional species‐level phylogenies of fungus‐farming ants and their fungal cultivars, which are necessary for understanding the evolutionary processes that gave rise to agriculture in ants and that produced the current diversity of mutualistic ant–fungus interactions.

     
    more » « less
  4. Abstract

    The Cyathocotylidae is a globally distributed family of digeneans parasitic as adults in fish, reptiles, birds and mammals in both freshwater and marine environments. Molecular phylogenetic analysis of interrelationships among cyathocotylids is lacking with only a few species included in previous studies. We used sequences of the nuclear 28S rRNA gene to examine phylogenetic affinities of 11 newly sequenced taxa of cyathocotylids and the closely related family Brauninidae collected from fish, reptiles, birds and dolphins from Australia, Southeast Asia, Europe, North America and South America. This is the first study to provide sequence data from adult cyathocotylids parasitic in fish and reptiles. Our analyses demonstrated that the members of the genusBraunina(family Brauninidae) belong to the Cyathocotylidae, placing the Brauninidae into synonymy with the Cyathocotylidae. In addition, our DNA sequences supported the presence of a second species in the currently monotypicBraunina. Our phylogeny revealed thatCyathocotylespp. from crocodilians belong to a separate genus (Suchocyathocotyle, previously proposed as a subgenus) and subfamily (Suchocyathocotylinae subfam. n.). Morphological study ofGogatea serpentum indicumsupported its elevation to species asGogatea mehri. The phylogeny did not supportHolostephanoideswithin the subfamily Cyathocotylinae; instead,Holostephanoidesformed a strongly supported clade with members of the subfamily Szidatiinae (GogateaandNeogogatea). Therefore, we transferHolostephanoidesinto the Szidatiinae. DNA sequence data revealed the potential presence of cryptic species reported under the nameMesostephanus microbursa. Our phylogeny indicated at least two major host switching events in the evolutionary history of the subfamily Szidatiinae which likely resulted in the transition of these parasites from birds to fish and snakes. Likewise, the transition to dolphins byBrauninarepresents another major host switching event among the Cyathocotylidae. In addition, our phylogeny revealed more than a single transition between freshwater and marine environments demonstrated in our dataset byBrauninaand someMesostephanus.

     
    more » « less
  5. Cavanaugh, Colleen M. (Ed.)
    ABSTRACT Diet and gut microbiomes are intricately linked on both short and long timescales. Changes in diet can alter the microbiome, while microbes in turn allow hosts to access novel diets. Bees are wasps that switched to a vegetarian lifestyle, and the vast majority of bees feed on pollen and nectar. Some stingless bee species, however, also collect carrion, and a few have fully reverted to a necrophagous lifestyle, relying on carrion for protein and forgoing flower visitation altogether. These “vulture” bees belong to the corbiculate apid clade, which is known for its ancient association with a small group of core microbiome phylotypes. Here, we investigate the vulture bee microbiome, along with closely related facultatively necrophagous and obligately pollinivorous species, to understand how these diets interact with microbiome structure. Via deep sequencing of the 16S rRNA gene and subsequent community analyses, we find that vulture bees have lost some core microbes, retained others, and entered into novel associations with acidophilic microbes found in the environment and on carrion. The abundance of acidophilic bacteria suggests that an acidic gut is important for vulture bee nutrition and health, as has been found in other carrion-feeding animals. Facultatively necrophagous bees have more variable microbiomes than strictly pollinivorous bees, suggesting that bee diet may interact with microbiomes on both short and long timescales. Further study of vulture bees promises to provide rich insights into the role of the microbiome in extreme diet switches. IMPORTANCE When asked where to find bees, people often picture fields of wildflowers. While true for almost all species, there is a group of specialized bees, also known as the vulture bees, that instead can be found slicing chunks of meat from carcasses in tropical rainforests. In this study, researchers compared the microbiomes of closely related bees that live in the same region but vary in their dietary lifestyles: some exclusively consume pollen and nectar, others exclusively depend on carrion for their protein, and some consume all of the above. Researchers found that vulture bees lost some ancestral “core” microbes, retained others, and entered into novel associations with acidophilic microbes, which have similarly been found in other carrion-feeding animals such as vultures, these bees’ namesake. This research expands our understanding of how diet interacts with microbiomes on both short and long timescales in one of the world’s biodiversity hot spots. 
    more » « less