scholarly journals Bacteria contribute to plant secondary compound degradation in a generalist herbivore system

2019 ◽  
Author(s):  
Charlotte B. Francoeur ◽  
Lily Khadempour ◽  
Rolando D. Moreira-Soto ◽  
Kirsten Gotting ◽  
Adam J. Book ◽  
...  

AbstractHerbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems, degrading the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. Here, we investigate the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome p450s and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we show that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using GC-MS, we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that sub-colonies of fungus gardens reduced α-pinene and linalool over a 36-hour period, while L. gongylophorus strains alone only reduced linalool. Overall, our results reveal that the bacterial community in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system.ImportanceLeaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their role in the detoxification of plant secondary compounds. Here, we assess if the bacterial community associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest the fungus garden and its associated microbial community influences the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Charlotte B. Francoeur ◽  
Lily Khadempour ◽  
Rolando D. Moreira-Soto ◽  
Kirsten Gotting ◽  
Adam J. Book ◽  
...  

ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus, the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria-dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ. Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus, Burkholderia, Enterobacter, Klebsiella, and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus. Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores.


mBio ◽  
2021 ◽  
Author(s):  
Charlotte B. Francoeur ◽  
Lily Khadempour ◽  
Rolando D. Moreira-Soto ◽  
Kirsten Gotting ◽  
Adam J. Book ◽  
...  

2001 ◽  
Vol 2001 ◽  
pp. 148-148
Author(s):  
A.J. Duncan ◽  
S.A. Young

Ruminants foraging under free-ranging conditions include a diversity of plants in their diet. A wide range of plant secondary compounds are broken down under microbial action in the rumen thus protecting the host animal from their otherwise toxic effects. For example, oxalic acid (OA), found in many tropical grasses, is effectively degraded by Oxalobacter formigenes following a period of adaptation of the rumen micro-flora (Allison et al, 1985). Similarly, butenyl nitrile (BN), a metabolite of glucosinolates, found in brassica plants, has been shown to degrade under rumen microbial action (Duncan & Milne, 1992). The purpose of this experiment was to investigate whether adaptation to the plant secondary compounds found in one food type might influence the degradation of other, unrelated secondary compounds and vice versa.


2020 ◽  
Vol 8 (9) ◽  
pp. 1311
Author(s):  
Chao Fan ◽  
Liangzhi Zhang ◽  
Haibo Fu ◽  
Chuanfa Liu ◽  
Wenjing Li ◽  
...  

Animal gut microbiomes can be clustered into “enterotypes” characterized by an abundance of signature genera. The characteristic determinants, stability, and resilience of these community clusters remain poorly understood. We used plateau pika (Ochotona curzoniae) as a model and identified three enterotypes by 16S rDNA sequencing. Among the top 15 genera, 13 showed significantly different levels of abundance between the enterotypes combined with different microbial functions and distinct fecal short-chain fatty acids. We monitored changes in the microbial community associated with the transfer of plateau pikas from field to laboratory and observed that feeding them a single diet reduced microbial diversity, resulting in a single enterotype with an altered composition of the dominant bacteria. However, microbial diversity, an abundance of some changed dominant genera, and enterotypes were partially restored after adding swainsonine (a plant secondary compound found in the natural diet of plateau pikas) to the feed. These results provide strong evidence that gut microbial diversity and enterotypes are directly related to specific diet, thereby indicating that the formation of different enterotypes can help animals adapt to complex food conditions. Additionally, natural plant secondary compounds can maintain dominant bacteria and inter-individual differences of gut microbiota and promote the resilience of enterotypes in small herbivorous mammals.


2002 ◽  
Vol 50 (5) ◽  
pp. 507 ◽  
Author(s):  
I. R. Wallis ◽  
M. L. Watson ◽  
W. J. Foley

We studied the influence of a group of plant secondary compounds, the sideroxylonals, on feeding by the common brushtail possum (Trichosurus vulpecula), a generalist herbivore. Possums were offered synthetic diets either with or without sideroxylonals or, in separate experiments, foliage from 28 individual Eucalyptus melliodora trees. Possums ate less of the synthetic diet at sideroxylonal concentrations of 4 and 7 mg g–1 when offered a choice or no choice, respectively. Possums fed foliage in no-choice protocols ate 12–61 g of dry matter per day. Sideroxylonal concentration was an essential determinant of feeding on foliage but the wide variation, particularly at intermediate sideroxylonal concentrations, suggests that other secondary plant chemicals, e.g. tannins, are important also. The normal distribution of sideroxylonal concentrations (mean = 27.7, s.d. = 7.85 mg sideroxylonals per g dry leaf) in a natural population of 150 E. melliodora trees shows that brushtail possums will rarely encounter highly palatable trees (<10 mg sideroxylonals per g dry leaf) nor highly unpalatable foliage (>40 mg sideroxylonals per g dry leaf). When foraging on E. melliodora, brushtail possums must contend with intermediate sideroxylonal concentrations (20–30 mg per g dry leaf), where variability in food intake is most noticeable.


Author(s):  
G.N. Hariharan ◽  
S. Karthik ◽  
S. Muthukumar

The mycobiont and whole thallus cultures of Roccella montagnei Bel. were established using soredia as an inoculum.The mycobiont cultures showed optimum growth, biomass and biosynthesis of compounds in Lilly and Barnett medium with glucose as a carbon source, micronutrients and vitamins. After the incubation period of 180 days, the cultures were harvested, and their biomass and secondary compound profiles were analysed. The HPTLC chromatogram of the acetone extract of the NT and mycobiont cultures revealed erythrinas the major biosynthesized compound in both and identified as a key biosynthate by R. montagnei. Further, the NT biosynthesized 5 additional compounds and themycobiont cultures biosynthesized 6 additional compounds. The molecular identity of the cultured mycobiont was confirmed using nuclear ribosomal Internal Transcribed Spacer (ITS) as well as the secondary chemistry. Lichen compound erythrin was identified as a key biosynthate by the cultures.


2020 ◽  
Vol 41 (S1) ◽  
pp. s258-s259
Author(s):  
James Harrigan ◽  
Ebbing Lautenbach ◽  
Emily Reesey ◽  
Magda Wernovsky ◽  
Pam Tolomeo ◽  
...  

Background: Clinically diagnosed ventilator-associated pneumonia (VAP) is common in the long-term acute-care hospital (LTACH) setting and may contribute to adverse ventilator-associated events (VAEs). Pseudomonas aeruginosa is a common causative organism of VAP. We evaluated the impact of respiratory P. aeruginosa colonization and bacterial community dominance, both diagnosed and undiagnosed, on subsequent P. aeruginosa VAP and VAE events during long-term acute care. Methods: We enrolled 83 patients on LTACH admission for ventilator weaning, performed longitudinal sampling of endotracheal aspirates followed by 16S rRNA gene sequencing (Illumina HiSeq), and bacterial community profiling (QIIME2). Statistical analysis was performed with R and Stan; mixed-effects models were fit to relate the abundance of respiratory Psa on admission to clinically diagnosed VAP and VAE events. Results: Of the 83 patients included, 12 were diagnosed with P. aeruginosa pneumonia during the 14 days prior to LTACH admission (known P. aeruginosa), and 22 additional patients received anti–P. aeruginosa antibiotics within 48 hours of admission (suspected P. aeruginosa); 49 patients had no known or suspected P. aeruginosa (unknown P. aeruginosa). Among the known P. aeruginosa group, all 12 patients had P. aeruginosa detectable by 16S sequencing, with elevated admission P. aeruginosa proportional abundance (median, 0.97; IQR, 0.33–1). Among the suspected P. aeruginosa group, all 22 patients had P. aeruginosa detectable by 16S sequencing, with a wide range of admission P. aeruginosa proportional abundance (median, 0.0088; IQR, 0.00012–0.31). Of the 49 patients in the unknown group, 47 also had detectable respiratory Psa, and many had high P. aeruginosa proportional abundance at admission (median, 0.014; IQR, 0.00025–0.52). Incident P. aeruginosa VAP was observed within 30 days in 4 of the known P. aeruginosa patients (33.3%), 5 of the suspected P. aeruginosa patients (22.7%), and 8 of the unknown P. aeruginosa patients (16.3%). VAE was observed within 30 days in 1 of the known P. aeruginosa patients (8.3%), 2 of the suspected P. aeruginosa patients (9.1%), and 1 of the unknown P. aeruginosa patients (2%). Admission P. aeruginosa abundance was positively associated with VAP and VAE risk in all groups, but the association only achieved statistical significance in the unknown group (type S error <0.002 for 30-day VAP and <0.011 for 30-day VAE). Conclusions: We identified a high prevalence of unrecognized respiratory P. aeruginosa colonization among patients admitted to LTACH for weaning from mechanical ventilation. The admission P. aeruginosa proportional abundance was strongly associated with increased risk of incident P. aeruginosa VAP among these patients.Funding: NoneDisclosures: None


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