Gut microbiota in an invasive bark beetle infected by a pathogenic fungus accelerates beetle mortality

The cosmopolitan insect-pathogenic fungus and popular biocontrol agent Beauveria bassiana can be used to control Anopheles mosquito populations and restrict the spread of malaria, the deadliest vector-borne infectious disease in the world caused by the protozoan parasite Plasmodium. Here, we establish that infection with a double-stranded (ds)RNA mycovirus, Beauveria bassiana polymycovirus (BbPmV)-1, significantly reduces B. bassiana virulence against A. coluzzii, the main vector of malaria. The BbPmV-1-mediated hypovirulence can be at least partially attributed to slow fungal growth on the mosquitos. Analysis of the dual next-generation sequencing of the B. bassiana and A. coluzzii transcriptomes provided insight into the molecular mechanisms of the BbPmV-1-mediated effects. BbPmV-1-free B. bassiana has a wide impact on the A. coluzzii transcriptome, affecting immunity and metabolism, and led to the identification of novel immune response proteins. BbPmV-1 regulates the gene expression profile of its fungal host, directing the use of available resources towards sporulation and suppressing the mosquito immune system. Additionally, BbPmV-1-infected and -free B. bassiana strains differentially modulate mosquito gut microbiota; the former reduces the bacterial genus Elizabethkingia and the latter Serratia. Co-transfection of mosquitos with B. bassiana and P. berghei revealed a reduction of ookinetes in the presence of BbPmV-1, potentially due to the upregulation of a mycotoxin. Finally, BbPmV-1-mediated hypovirulence is at least partially dependent on the A. coluzzii RNAi pathway, and silencing of the dicer-2 gene restores virulence. Taken together, our data clearly demonstrate the crucial role of mycovirus infection in mediating B. bassiana virulence against A. coluzzii and suggest that BbPmV-1 protects A. coluzzii from B. bassiana, the mosquito’s own immune system, potentially harmful gut microbiota, and Plasmodium parasites.

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Faculty Opinions recommendation of Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.727641761.793532577 ◽

2017 ◽

Author(s):

Weiqing Pan ◽

Qingfeng Zhang

Keyword(s):

Gut Microbiota ◽

Pathogenic Fungus ◽

Mosquito Mortality

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Insect pathogenic fungus interacts with the gut microbiota to accelerate mosquito mortality

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1703546114 ◽

2017 ◽

Vol 114 (23) ◽

pp. 5994-5999 ◽

Cited By ~ 80

Author(s):

Ge Wei ◽

Yiling Lai ◽

Guandong Wang ◽

Huan Chen ◽

Fang Li ◽

...

Keyword(s):

Gut Microbiota ◽

Fungal Infection ◽

Entomopathogenic Fungi ◽

Pathogenic Fungus ◽

Bacterial Load ◽

Mosquito Mortality ◽

Dual Oxidase ◽

Intestinal Pathogens ◽

Insect Gut ◽

Opportunistic Pathogenic

The insect gut microbiota plays crucial roles in modulating the interactions between the host and intestinal pathogens. Unlike viruses, bacteria, and parasites, which need to be ingested to cause disease, entomopathogenic fungi infect insects through the cuticle and proliferate in the hemolymph. However, interactions between the gut microbiota and entomopathogenic fungi are unknown. Here we show that the pathogenic fungus Beauveria bassiana interacts with the gut microbiota to accelerate mosquito death. After topical fungal infection, mosquitoes with gut microbiota die significantly faster than mosquitoes without microbiota. Furthermore, fungal infection causes dysbiosis of mosquito gut microbiota with a significant increase in gut bacterial load and a significant decrease in bacterial diversity. In particular, the opportunistic pathogenic bacterium Serratia marcescens overgrows in the midgut and translocates to the hemocoel, which promotes fungal killing of mosquitoes. We further reveal that fungal infection down-regulates antimicrobial peptide and dual oxidase expression in the midgut. Duox down-regulation in the midgut is mediated by secretion of the toxin oosporein from B. bassiana. Our findings reveal the important contribution of the gut microbiota in B. bassiana-killing activity, providing new insights into the mechanisms of fungal pathogenesis in insects.

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Fungal associates of five bark beetle species colonizing Norway spruce

Canadian Journal of Forest Research ◽

10.1139/x26-240 ◽

1996 ◽

Vol 26 (12) ◽

pp. 2115-2122 ◽

Cited By ~ 63

Author(s):

Paal Krokene ◽

Halvor Solheim

Keyword(s):

Norway Spruce ◽

Bark Beetle ◽

Bark Beetles ◽

Pathogenic Fungus ◽

Pathogenic Fungi ◽

Beetle Species ◽

Low Frequencies ◽

Blue Stain Fungi ◽

Blue Stain ◽

Fungal Associates

Fungi associated with five bark beetle species colonizing Norway spruce (Piceaabies (L.) Karst.) were isolated from beetle-inoculated logs. Ipstypographus L., an aggressive tree-killing bark beetle, was associated with a different range of blue-stain fungi than the nonaggressive Pityogeneschalcographus L., Polygraphuspoligraphus L., and Hylurgopspalliatus Gyll. The flora of the nonaggressive Ipsduplicatus Sahib. was similar to that of I. typographus. The pathogenic fungus Ceratocystispolonica (Siem.) C. Moreau, and other blue-stain fungi, were isolated in high frequency from inoculations with both Ips species. Pathogenic blue-stain fungi were absent, or isolated in low frequencies, from inoculations with the other nonaggressive beetle species. With the exception of I. duplicatus, these results support the hypothesis that aggressive bark beetles carry more pathogenic blue-stain fungi than other bark beetles and indicate that pathogenic fungi are important for aggressive bark beetles to kill trees.

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Pine engraver beetle Ips acuminatus as a potential vector of Sphaeropsis sapinea

Forestry and Forest Melioration ◽

10.33220/1026-3365.136.2020.149 ◽

2020 ◽

pp. 149-156

Author(s):

K. V. Davydenko ◽

D. O. Baturkin

Keyword(s):

Bark Beetle ◽

Pathogenic Fungus ◽

Opportunistic Pathogen ◽

Potential Vector ◽

Pine Engraver ◽

Sphaeropsis Sapinea ◽

Pine Engraver Beetle

The pine engraver beetle Ips acuminatus Gyll. is a potential vector of the Sphaeropsis tip blight pathogen according to Leach’s postulates. The specimens of I. acuminatus were associated with numerous fungi species, namely Sphaeropsis sapinea (Fr.) Dyko & B. Sutton and ophiostomatoid species. The association between opportunistic pathogen S. sapinea and I. acuminatus has been confirmed for 62.9 % of all branches (44 % of needle samples and 82 % of wood samples). The presence of S. sapinea in the galleries and on the surface of the beetle indicates that I. acuminatus may transport the pathogen and later introduce it into healthy trees. The bark beetle can transfer pathogenic fungus during maturation feeding on the shoots of healthy pine crowns and into the branches during making galleries.

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High-pressure freezing and freeze substitution of teliospores of the rust fungus Gymnosporangium clavipes

Proceedings, annual meeting, Electron Microscopy Society of America ◽

10.1017/s0424820100161011 ◽

1990 ◽

Vol 48 (3) ◽

pp. 692-693

Author(s):

Robert W. Roberson

Keyword(s):

High Pressure ◽

Room Temperature ◽

Pathogenic Fungus ◽

Rust Fungus ◽

Freeze Substitution ◽

Ice Crystals ◽

High Pressure Freezing ◽

Thin Walled Structures ◽

Cytological Changes ◽

Dextran Solution

The use of cryo-techniques for the preparation of biological specimens in electron microscopy has led to superior preservation of ultrastructural detail. Although these techniques have obvious advantages, a critical limitation is that only 10-40 μm thick cells and tissue layers can be frozen without the formation of distorting ice crystals. However, thicker samples (600 μm) may be frozen well by rapid freezing under high-pressure (2,100 bar). To date, most work using cryo-techniques on fungi have been confined to examining small, thin-walled structures. High-pressure freezing and freeze substitution are used here to analysis pre-germination stages of specialized, sexual spores (teliospores) of the plant pathogenic fungus Gymnosporangium clavipes C & P.Dormant teliospores were incubated in drops of water at room temperature (25°C) to break dormancy and stimulate germination. Spores were collected at approximately 30 min intervals after hydration so that early cytological changes associated with spore germination could be monitored. Prior to high-pressure freezing, the samples were incubated for 5-10 min in a 20% dextran solution for added cryoprotection during freezing. Forty to 50 spores were placed in specimen cups and holders and immediately frozen at high pressure using the Balzers HPM 010 apparatus.

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