scholarly journals Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System

mBio ◽  
2020 ◽  
Vol 11 (5) ◽  
Author(s):  
Charlotte B. Francoeur ◽  
Lily Khadempour ◽  
Rolando D. Moreira-Soto ◽  
Kirsten Gotting ◽  
Adam J. Book ◽  
...  
Keyword(s):  
Bacterial Community ◽  
Bacterial Communities ◽  
Secondary Compounds ◽  
Fungus Garden ◽  
Plant Secondary Compounds ◽  
Generalist Herbivore ◽  
Secondary Compound ◽  
Wide Range ◽  
Plant Secondary Compound ◽  
Microbial Symbionts

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.

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 ◽  
...  
Keyword(s):  
Bacterial Community ◽  
Secondary Compounds ◽  
Fungus Garden ◽  
Ant System ◽  
Plant Secondary Compounds ◽  
Generalist Herbivore ◽  
Secondary Compound ◽  
Wide Range ◽  
Plant Secondary Compound ◽  
Microbial Symbionts

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.

scholarly journals Erratum for Francoeur et al., “Bacteria Contribute to Plant Secondary Compound Degradation in a Generalist Herbivore System”

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

scholarly journals Metagenomics reveals diet-specific specialization of bacterial communities in fungus gardens of grass- and dicot-cutter ants

2018 ◽  
Author(s):  
Lily Khadempour ◽  
Huan Fan ◽  
Ken Keefover-Ring ◽  
Camila Carlos ◽  
Nilson S. Nagamoto ◽  
...  
Keyword(s):  
Bacterial Community ◽  
Community Composition ◽  
Bacterial Communities ◽  
Potential Role ◽  
Sequence Data ◽  
Bacterial Community Composition ◽  
Fungus Garden ◽  
Functional Profiles ◽  
Ant Fungus

AbstractLeaf-cutter ants in the genusAttaare dominant herbivores in the Neotropics. While most species ofAttacut dicots to incorporate into their fungus gardens, some species specialize on grasses. Here we examine the bacterial community associated with the fungus gardens of grass- and dicot-cutter ants to examine how changes in substrate input affect the bacterial community. We sequenced the metagenomes of 12Attafungus gardens, across four species of ants, with a total of 5.316 Gbp of sequence data. We show significant differences in the fungus garden bacterial community composition between dicot- and grass-cutter ants, with grass-cutter ants having lower diversity. Reflecting this difference in community composition, the bacterial functional profiles between the fungus gardens are significantly different. Specifically, grass-cutter ant fungus garden metagenomes are particularly enriched for genes responsible for amino acid, siderophore, and terpenoid biosynthesis while dicot-cutter ant fungus gardens metagenomes are enriched in genes involved in membrane transport. These differences in bacterial community composition and functional capacity show that different substrate inputs matter for fungus garden bacteria, and sheds light on the potential role of bacteria in mediating the ants’ transition to the use of a novel substrate.

scholarly journals Robust Hydrocarbon Degradation and Dynamics of Bacterial Communities during Nutrient-Enhanced Oil Spill Bioremediation

2002 ◽  
Vol 68 (11) ◽  
pp. 5537-5548 ◽  
Author(s):  
Wilfred F. M. Röling ◽  
Michael G. Milner ◽  
D. Martin Jones ◽  
Kenneth Lee ◽  
Fabien Daniel ◽  
...  
Keyword(s):  
Bacterial Community ◽  
16S Rrna ◽  
Oil Spill ◽  
Bacterial Communities ◽  
Inorganic Nutrients ◽  
16S Rrna Genes ◽  
Rrna Genes ◽  
Oil Degradation ◽  
Beach Sediment ◽  
Wide Range

ABSTRACT Degradation of oil on beaches is, in general, limited by the supply of inorganic nutrients. In order to obtain a more systematic understanding of the effects of nutrient addition on oil spill bioremediation, beach sediment microcosms contaminated with oil were treated with different levels of inorganic nutrients. Oil biodegradation was assessed respirometrically and on the basis of changes in oil composition. Bacterial communities were compared by numerical analysis of denaturing gradient gel electrophoresis (DGGE) profiles of PCR-amplified 16S rRNA genes and cloning and sequencing of PCR-amplified 16S rRNA genes. Nutrient amendment over a wide range of concentrations significantly improved oil degradation, confirming that N and P limited degradation over the concentration range tested. However, the extent and rate of oil degradation were similar for all microcosms, indicating that, in this experiment, it was the addition of inorganic nutrients rather than the precise amount that was most important operationally. Very different microbial communities were selected in all of the microcosms. Similarities between DGGE profiles of replicate samples from a single microcosm were high (95% ± 5%), but similarities between DGGE profiles from replicate microcosms receiving the same level of inorganic nutrients (68% ± 5%) were not significantly higher than those between microcosms subjected to different nutrient amendments (63% ± 7%). Therefore, it is apparent that the different communities selected cannot be attributed to the level of inorganic nutrients present in different microcosms. Bioremediation treatments dramatically reduced the diversity of the bacterial community. The decrease in diversity could be accounted for by a strong selection for bacteria belonging to the alkane-degrading Alcanivorax/Fundibacter group. On the basis of Shannon-Weaver indices, rapid recovery of the bacterial community diversity to preoiling levels of diversity occurred. However, although the overall diversity was similar, there were considerable qualitative differences in the community structure before and after the bioremediation treatments.

Rumen microbial breakdown of plant secondary compounds in ruminants consuming mixed diets

2001 ◽  
Vol 2001 ◽  
pp. 148-148
Author(s):  
A.J. Duncan ◽  
S.A. Young
Keyword(s):  
Oxalic Acid ◽  
Secondary Compounds ◽  
Food Type ◽  
Oxalobacter Formigenes ◽  
Plant Secondary Compounds ◽  
Host Animal ◽  
Tropical Grasses ◽  
Wide Range ◽  
Free Ranging ◽  
Microbial Action

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.

scholarly journals Enterotypes of the Gut Microbial Community and Their Response to Plant Secondary Compounds in Plateau Pikas

2020 ◽  
Vol 8 (9) ◽  
pp. 1311
Author(s):  
Chao Fan ◽  
Liangzhi Zhang ◽  
Haibo Fu ◽  
Chuanfa Liu ◽  
Wenjing Li ◽  
...  
Keyword(s):  
Microbial Community ◽  
Microbial Diversity ◽  
Secondary Compounds ◽  
Short Chain Fatty Acids ◽  
Plant Secondary Compounds ◽  
Plateau Pika ◽  
Natural Diet ◽  
Rdna Sequencing ◽  
Plant Secondary Compound ◽  
Dominant Bacteria

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.

Secondary metabolites in Eucalyptus melliodora: field distribution and laboratory feeding choices by a generalist herbivore, the common brushtail possum

2002 ◽  
Vol 50 (5) ◽  
pp. 507 ◽  
Author(s):  
I. R. Wallis ◽  
M. L. Watson ◽  
W. J. Foley
Keyword(s):  
Dry Matter ◽  
Secondary Compounds ◽  
Brushtail Possum ◽  
Trichosurus Vulpecula ◽  
Plant Secondary Compounds ◽  
Generalist Herbivore ◽  
Plant Chemicals ◽  
The Common ◽  
Common Brushtail Possum ◽  
Feeding Choices

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.

Mycobiont and Whole Thallus Cultures of Roccella Montagnei Bél. For the Biosynthesis of Secondary Compounds

2016 ◽  
Vol 1 (1) ◽  
Author(s):  
G.N. Hariharan ◽  
S. Karthik ◽  
S. Muthukumar
Keyword(s):  
Carbon Source ◽  
Incubation Period ◽  
Internal Transcribed Spacer ◽  
Secondary Compounds ◽  
Acetone Extract ◽  
Optimum Growth ◽  
Secondary Chemistry ◽  
Molecular Identity ◽  
Secondary Compound

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.

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