New mycoparasitic species in the genera Niveomyces and Pseudoniveomycesgen. nov. (Hypocreales: Cordycipitaceae), with sporothrix-like asexual morphs, from Thailand.

Four new species of the genus Niveomyces are described from Thailand. They were found as mycoparasites on: Ophiocordyceps infecting flies (Diptera) for Niveomyces albus; ants (Hymenoptera) for N. formicidarum; and leafhoppers (Hemiptera) for N. hirsutellae and N. multisynnematus. A new genus, Pseudoniveomyces with two species: Pseudoniveo. blattae (type species), parasitic on Ophiocordyceps infecting cockroaches, and Pseudoniveo. arachnovorum, found on a spider egg sac, are also described. These fungi share a common feature which is a sporothrix-like asexual morph. Based on our molecular data, Sporothrix insectorum is shown to be affiliated to the genus Niveomyces, and thus a new combination N. insectorum comb. nov. is proposed. Niveomyces coronatus, N. formicidarum and N. insectorum formed the N. coronatus species complex found on ant-pathogenic Ophiocordyceps from different continents. Pseudoniveomyces species are distinguished from Niveomyces spp. based on the presence of fusoid macroconidia in culture and a red pigment diffused in the medium, resembling to Gibellula and Hevansia. The molecular phylogenetic analyses also confirmed its generic status. The host/substrates associated with the genera within Cordycipitaceae were mapped onto the phylogeny to demonstrate that mycoparasitism also evolved independently multiple times in this family. Citation: Kobmoo N, Tasanathai K, Araújo JPM, Noisripoom W, Thanakitpipattana D, Mongkolsamrit S, Himaman W, Houbraken J, Luangsa-ard JJ (2023). New mycoparasitic species in the genera Niveomyces and Pseudoniveomyces gen. nov. (Hypocreales: Cordycipitaceae), with sporothrix-like asexual morphs, from Thailand. Fungal Systematics and Evolution 12: 91-110. doi: 10.3114/fuse.2023.12.07.

Masters of the manipulator: two new hypocrealean genera, Niveomyces (Cordycipitaceae) and Torrubiellomyces (Ophiocordycipitaceae), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani.

During surveys in central Florida of the zombie-ant fungus Ophiocordyceps camponoti-floridani, which manipulates the behavior of the carpenter ant Camponotus floridanus, two distinct fungal morphotypes were discovered associated with and purportedly parasitic on O. camponoti-floridani. Based on a combination of unique morphology, ecology and phylogenetic placement, we discovered that these morphotypes comprise two novel lineages of fungi. Here, we propose two new genera, Niveomyces and Torrubiellomyces, each including a single species within the families Cordycipitaceae and Ophiocordycipitaceae, respectively. We generated de novo draft genomes for both new species and performed morphological and multi-loci phylogenetic analyses. The macromorphology and incidence of both new species, Niveomyces coronatus and Torrubiellomyces zombiae, suggest that these fungi are mycoparasites since their growth is observed exclusively on O. camponoti-floridani mycelium, stalks and ascomata, causing evident degradation of their fungal hosts. This work provides a starting point for more studies into fungal interactions between mycopathogens and entomopathogens, which have the potential to contribute towards efforts to battle the global rise of plant and animal mycoses. Citation: Araújo JPM, Lebert BM, Vermeulen S, et al. 2022. Masters of the manipulator: two new hypocrealean general, Niveomyces (Cordycipitaceae) and Torrubiellomyces (Ophiocordycipitaceae), parasitic on the zombie ant fungus Ophiocordyceps camponoti-floridani. Persoonia 49: 171-194. https://doi.org/10.3767/persoonia.2022.49.05.

Fusarium: more than a node or a foot-shaped basal cell.

Recent publications have argued that there are potentially serious consequences for researchers in recognising distinct genera in the terminal fusarioid clade of the family Nectriaceae. Thus, an alternate hypothesis, namely a very broad concept of the genus Fusarium was proposed. In doing so, however, a significant body of data that supports distinct genera in Nectriaceae based on morphology, biology, and phylogeny is disregarded. A DNA phylogeny based on 19 orthologous protein-coding genes was presented to support a very broad concept of Fusarium at the F1 node in Nectriaceae. Here, we demonstrate that re-analyses of this dataset show that all 19 genes support the F3 node that represents Fusarium sensu stricto as defined by F. sambucinum (sexual morph synonym Gibberella pulicaris). The backbone of the phylogeny is resolved by the concatenated alignment, but only six of the 19 genes fully support the F1 node, representing the broad circumscription of Fusarium. Furthermore, a re-analysis of the concatenated dataset revealed alternate topologies in different phylogenetic algorithms, highlighting the deep divergence and unresolved placement of various Nectriaceae lineages proposed as members of Fusarium. Species of Fusarium s. str. are characterised by Gibberella sexual morphs, asexual morphs with thin- or thick-walled macroconidia that have variously shaped apical and basal cells, and trichothecene mycotoxin production, which separates them from other fusarioid genera. Here we show that the Wollenweber concept of Fusarium presently accounts for 20 segregate genera with clear-cut synapomorphic traits, and that fusarioid macroconidia represent a character that has been gained or lost multiple times throughout Nectriaceae. Thus, the very broad circumscription of Fusarium is blurry and without apparent synapomorphies, and does not include all genera with fusarium-like macroconidia, which are spread throughout Nectriaceae (e.g., Cosmosporella, Macroconia, Microcera). In this study four new genera are introduced, along with 18 new species and 16 new combinations. These names convey information about relationships, morphology, and ecological preference that would otherwise be lost in a broader definition of Fusarium. To assist users to correctly identify fusarioid genera and species, we introduce a new online identification database, Fusarioid-ID, accessible at www.fusarium.org. The database comprises partial sequences from multiple genes commonly used to identify fusarioid taxa (act1, CaM, his3, rpb1, rpb2, tef1, tub2, ITS, and LSU). In this paper, we also present a nomenclator of names that have been introduced in Fusarium up to January 2021 as well as their current status, types, and diagnostic DNA barcode data. In this study, researchers from 46 countries, representing taxonomists, plant pathologists, medical mycologists, quarantine officials, regulatory agencies, and students, strongly support the application and use of a more precisely delimited Fusarium (= Gibberella) concept to accommodate taxa from the robust monophyletic node F3 on the basis of a well-defined and unique combination of morphological and biochemical features. This F3 node includes, among others, species of the F. fujikuroi, F. incarnatum-equiseti, F. oxysporum, and F. sambucinum species complexes, but not species of Bisifusarium [F. dimerum species complex (SC)], Cyanonectria (F. buxicola SC), Geejayessia (F. staphyleae SC), Neocosmospora (F. solani SC) or Rectifusarium (F. ventricosum SC). The present study represents the first step to generating a new online monograph of Fusarium and allied fusarioid genera (www.fusarium.org).

Zombie-ant fungi cross continents: II. Myrmecophilous hymenostilboid species and a novel zombie lineage.

Ophiocordyceps species infecting ants are globally distributed, with diversity concentrated in the tropics and decreasing with increasing latitude. Among these myrmecophilous species, the ones exhibiting the ability to manipulate host behavior, the so-called "zombie-ant fungi" of the O. unilateralis clade, have been studied progressively over the last decade. However, we know very little about other myrmecophilous groups, such as species within the Ophiocordyceps subgenus Neocordyceps. Species within this group exhibit Hymenostilbe asexual morphs with the ascospores readily breaking into part-spores and regularly kill their hosts on the forest floor, with few records of behavioral manipulation. Here, we describe five new species of Ophiocordyceps belonging to the subgenus Neocordyceps infecting ants in the rainforests of the Brazilian Amazon and Ghana and analyze their ability to manipulate host behavior. We also propose a new status for a species previously described as a variety, providing its phylogenetic placement for the first time. The species proposed herein can readily be separated using classic taxonomic criteria, and this is further supported by ecological and molecular multiloci data.

Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species.

Ophiocordyceps species infecting ants - the so-called zombie-ant fungi - comprise one of the most intriguing and fascinating relationships between microbes and animals. They are widespread within tropical forests worldwide, with relatively few reports from temperate ecosystems. These pathogens possess the ability to manipulate host behaviour in order to increase their own fitness. Depending on the fungal species involved the infected ants are manipulated either to leave the nest to ascend understorey shrubs, to die biting onto vegetation, or descend from the canopy to die at the base of trees. Experimental evidence has demonstrated that the behavioural change aids spore dispersal and thus increases the chances of infection, because of the existing behavioural immunity expressed inside ant colonies that limits fungal development and transmission. Despite their undoubted importance for ecosystem functioning, these fungal pathogens are still poorly documented, especially regarding their diversity, ecology and evolutionary relationships. Here, we describe 15 new species of Ophiocordyceps with hirsutella-like asexual morphs that exclusively infect ants. These form a monophyletic group that we identified in this study as myrmecophilous hirsutelloid species. We also propose new combinations for species previously described as varieties and provide for the first time important morphological and ecological information. The species proposed herein were collected in Brazil, Colombia, USA, Australia and Japan. All species could readily be separated using classic taxonomic criteria, in particular ascospore and asexual morphology.

Epitypification and re-description of the zombie-ant fungus, Ophiocordyceps unilateralis (Ophiocordycipitaceae).

The type of Ophiocordyceps unilateralis (Ophiocordycipitaceae, Hypocreales, Ascomycota) is based on an immature specimen collected on an ant in Brazil. The host was identified initially as a leaf-cutting ant (Atta cephalotes, Attini, Myrmicinae). However, a critical examination of the original illustration reveals that the host is the golden carpenter ant, Camponotus sericeiventris (Camponotini, Formicinae). Because the holotype is no longer extant and the original diagnosis lacks critical taxonomic information - specifically, on ascus and ascospore morphology - a new type from Minas Gerais State of south-east Brazil is designated herein. A re-description of the fungus is provided and a new phylogenetic tree of the O. unilateralis clade is presented. It is predicted that many more species of zombie-ant fungi remain to be delimited within the O. unilateralis complex worldwide, on ants of the tribe Camponotini.

Diversity of Entomopathogenic Fungi: Which Groups Conquered the Insect Body?

The entomopathogenic fungi are organisms that evolved to exploit insects. They comprise a wide range of morphologically, phylogenetically, and ecologically diverse fungal species. Entomopathogenic fungi can be found distributed among five of the eight fungal phyla. Entomopathogens are also present among the ecologically similar but phylogenetically distinct Oomycota or water molds, which belong to a different kingdom, the Stramenopila. As a group of parasites, the entomopathogenic fungi and water molds infect a wide range of insect hosts, from aquatic larvae to adult insects from high canopies in tropical forests or even deserts. Their hosts are spread among 20 of the 31 orders of insects, in all developmental stages: eggs, larvae, pupae, nymphs, and adults. Such assortment of niches has resulted in these parasites evolving a considerable morphological diversity, resulting in enormous biodiversity, the majority of which remains unknown. Here we undertake a comprehensive survey of records of these entomopathogens in order to compare and contrast both their morphologies and their ecological traits. Our findings highlight a wide range of adaptations that evolved following the evolutionary transition by the fungi and water molds to infect the most diverse and widespread animals on Earth, the insects.

From So Simple a Beginning: The Evolution of Behavioral Manipulation by Fungi.

Parasites can manipulate the behavior of their hosts in ways that increase either their direct fitness or transmission to new hosts. The Kingdom Fungi have evolved a diverse array of strategies to manipulate arthropod behavior resulting in some of the most complex and impressive examples of behavioral manipulation by parasites. Here we provide an overview of these different interactions and discuss them from an evolutionary perspective. We discuss parasite manipulation within the context of Niko Tinbergen's four questions (function, phylogeny, causation, and ontogeny) before detailing the proximate mechanisms by which fungi control arthropod behavior and the evolutionary pathways to such adaptations. We focus on some systems for which we have recently acquired new knowledge (such as the zombie ant fungus, Ophiocordyceps unilateralis s.l.), but a major goal is also to highlight how many interesting examples remain to be discovered and investigated. With this in mind, we also discuss likely examples of manipulated spiders that are largely unexplored ("zombie spiders"). Armed with advanced tools in evolutionary biology (from serial block face SEM to RNAseq) we can discover how the fungi, a group of microbes capable of coordinated activity, have evolved the ability to direct animal behavior. In short, we have the ability to understand how the organism without the brain controls the one with the brain. We hope such a goal, coupled with the knowledge that many diverse examples of control exist, will inspire other organismal biologists to study the complex adaptations that have arisen from "so simple a beginning."