No abstract

In 1970 a corn disease epidemic ravaged fields in the United States to great economic loss. The outbreak was caused by a never-before seen, supervirulent strain of the fungal pathogen Cochliobolus heterostrophus. This was a plant disease epidemic, however, the current COVID-19 pandemic of humans is a stark reminder that novel, highly virulent, pathogens evolve with devastating consequences, no matter what the host-animal, plant, or other organism.

The microsporidian, Nosema maddoxi Becnel, Solter, Hajek, Huang, Sanscrainte & Estep, infects brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), populations in North America and Asia and causes decreased fitness in infected insects. This host overwinters as adults, often in aggregations in sheltered locations, and variable levels of mortality occur over the winter. We investigated pathogen prevalence in H. halys adults before, during, and after overwintering. Population level studies resulted in detection of N. maddoxi in H. halys in 6 new US states, but no difference in levels of infection by N. maddoxi in autumn versus the following spring. Halyomorpha halys that self-aggregated for overwintering in shelters deployed in the field were maintained under simulated winter conditions (4°C) for 5 months during the 2021–2022 winter and early spring, resulting in 34.6 ± 4.8% mortality. Over the 2020–2021 and 2021–2022 winters, 13.4 ± 3.5% of surviving H. halys in shelters were infected with N. maddoxi, while N. maddoxi infections were found in 33.4 ± 10.8% of moribund and dead H. halys that accumulated in shelters. A second pathogen, Colletotrichum fioriniae Marcelino & Gouli, not previously reported from H. halys, was found among 46.7 ± 7.8% of the H. halys that died while overwintering, but levels of infection decreased after overwintering. These 2 pathogens occurred as co-infections in 11.1 ± 5.9% of the fungal-infected insects that died while overwintering. Increasing levels of N. maddoxi infection caused epizootics among H. halys reared in greenhouse cages after overwintering.

In 1970, the Southern Corn Leaf Blight epidemic ravaged US fields to great economic loss. The outbreak was caused by never-before-seen, super-virulent, Race T of the fungus Cochliobolus heterostrophus. The functional difference between Race T and O, the previously known, far less aggressive strain, is production of T-toxin, a host-selective polyketide. Super-virulence is associated with ~1 Mb of Race T-specific DNA; only a fraction encodes T-toxin biosynthetic genes (Tox1). Tox1 is genetically and physically complex, with unlinked loci (Tox1A, Tox1B) genetically inseparable from breakpoints of a Race O reciprocal translocation that generated hybrid Race T chromosomes. Previously, we identified ten genes for T-toxin biosynthesis. Unfortunately, high depth, short-read sequencing placed these genes on four small, unconnected scaffolds surrounded by repeated A+T rich sequence, concealing context. To sort out Tox1 topology and pinpoint the hypothetical Race O translocation breakpoints corresponding to Race T-specific insertions, we undertook PacBio long-read sequencing which revealed Tox1 gene arrangement and the breakpoints. Six Tox1A genes are arranged as three small islands in a Race T-specific sea (~634 kb) of repeats. Four Tox1B genes are linked, on a large loop of Race T-specific DNA (~210 kb). The race O breakpoints are short sequences of race O-specific DNA; corresponding positions in race T are large insertions of race T-specific, A+T rich DNA, often with similarity to transposable (predominantly Gypsy) elements. Nearby, are 'Voyager Starship' elements and DUF proteins. These elements may have facilitated Tox1 integration into progenitor Race O and promoted large scale recombination resulting in race T.