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

Abstract

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.

Keywords: Hypocreales; behaviour manipulation; entomopathogenic fungi; genomics; mycoparasites; new taxa; taxonomy.

Fig. 1

Mycoparasites of Ophiocordyceps species pathogenic on Camponotini ants. a-b. Niveomyces-like growth on Ophiocordyceps camponoti-novogranadensison its host, Camponotusnovogranadensis, in Atlantic rainforest, Itacolomi, Minas Gerais, Brazil (Note yellow perithecia on the subiculum in b; c-d. on O. camponoti-rufipedis on Camponotus rufipes in Atlantic rainforest, Viposa, Minas Gerais, Brazil; e. torrubiellomyces-like perithecia on Ophiocordyceps camponoti-novogranadensis on, Camponotus novogranadensis, habitat as a, b; f. dark perithecia produced on the mycelium of Ophiocordyceps oecophyllae, on Oecophylla smaragdina in rainforest, Licuala State Forest, Queensland, Australia.

Fig. 2

Maximum likelihood tree of Cordycipitaceae obtained with a concatenated dataset of SSU, LSU, TEF, RPB1 and RPB2. Niveomyces gen. nov. is indicated in bold font. The whole analysis tree of the order Hypocreales is depicted in the top-right corner, with the position of Cordycipitaceae highlighted in red.

Fig. 3

Maximum likelihood tree of Ophiocordycipitaceae obtained with a concatenated dataset of SSU, LSU, TEF, RPB1 and RPB2. Torrubiellomyces gen. nov. is indicated in bold font. The host of Niveomyces and Torrubiellomyces, O. camponoti-floridani, is indicated in red. The whole analysis tree of the order Hypocreales is depicted in the top-right corner, with the position of Ophiocordycipitaceae highlighted in red.

Fig. 4

Niveomyces coronatus growing on Ophiocordyceps camponoti-floridani, a pathogen of the ant Camponotus floridanus. a. View of the tri-trophic system ant-entomopathogenic fungi-mycoparasite; b. close-up of N. coronatus synnemata; c. PDA culture after 60 d; d. close-up of culture edge; e. close-up of sporodochia formed in culture; f. layer of phialides (hymenium); g. close-up of apical and lateral conidiogenous cells; h. conidium. — Scale bars: f-g = 10 μm, h = 5 μm.

Fig. 5

Torrubiellomyces zombiae growing on Ophiocordyceps camponoti-floridani, a pathogen of the ant Camponotus floridanus. a. Close-up showing perithecia emerging from the antennal plate of the ant; b. general overview of a typical perithecial arrangement in clusters or less often singly produced; c-e. perithecia; f. mature ascospores disarticulated prior to release, forming corn cob-like asci; g. cluster of part-spores; h. ascus showing the ascospores already sub-divided into part-spores. — Scale bars: c-d = 100 μm, e = 50 μm, f = 10 μm, g-h = 5 μm.

Fig. 6

Torrubiellomyces zombiae in culture. a. PDA plate after 60 d, arrows indicate the pools of viscous conidia produced in sporodochia scattered over the plate; b. overview of the specimen, white arrows indicate T. zombiae perithecia emerging from the fungal host tissue; c. close-up of sporodochium with pools of viscous conidia; d. conidia; e. cluster of phialides; f—l. phialides. — Scale bars: c = 1000 μm, d = 3 μm, e = 20 μm, f-l = 5 μm.