Symbiotic solutions to nitrogen limitation and amino acid imbalance in insect diets

Hansen, Allison K.; Pers, Daniel; Russell, Jacob A.

doi:10.1016/bs.aiip.2020.03.001

Cited by 34 publications

(39 citation statements)

References 179 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…For fiber catabolism and N-recycling pathways (reviewed in [98, 99]), deemed to be of known [58], or likely, importance for these symbioses, we examined the reliability of functional annotations in IMG/M-ER by comparing these to results from two BLASTp searches performed for each retained search-returned gene – one against the SWISS-PROT database and the second against the NCBI nr database.…”

Section: Methodsmentioning

confidence: 99%

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

Béchade

Sanders

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Gut bacterial symbionts can support animal nutrition by facilitating digestion and providing valuable metabolites. While the composition of gut symbiont communities shifts with host development in holometabolous insects, changes in symbiotic roles between immature and adult stages are not well documented, especially in ants. Here, we explored the metabolic capabilities of microbiomes sampled from herbivorous turtle ant (Cephalotes sp.) larvae and adult workers through genomic and metagenomic screenings and targeted in vitro metabolic assays. We reveal that larval guts harbor bacterial symbionts from the Enterobacteriales, Lactobacillales and Rhizobiales orders, with impressive metabolic capabilities, including catabolism of plant and fungal recalcitrant fibers common in turtle ant diets, and energy-generating fermentation. Additionally, several members of the specialized turtle ant adult gut microbiome, sampled downstream of an anatomical barrier that dams large food particles, show a conserved potential to depolymerize many dietary fibers and other carbohydrates. Symbionts from both life stages have the genomic capacity to recycle nitrogen, synthesize amino acids and B-vitamins, and perform several key aspects of sulfur metabolism. We also document, for the first time in ants, an adult-associated Campylobacterales symbiont with an apparent capacity to anaerobically oxidize sulfide, reduce nitrate, and fix carbon dioxide. With help of their gut symbionts, including several bacteria likely acquired from the environment, turtle ant larvae appear as an important component of turtle ant colony digestion and nutrition. In addition, the conserved nature of the digestive, energy-generating, and nutritive capacities among adult-enriched symbionts suggests that nutritional ecology of turtle ant colonies has long been shaped by specialized, behaviorally-transferred gut bacteria with over 46 million years of residency.

show abstract

Section: Methodsmentioning

confidence: 99%

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

Béchade

Sanders

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…Gut microbiomes of insects can improve host fitness through a variety of mechanisms, ranging from detoxification [126,127], to defense [4], and to a series of nutrient-themed functions. These latter benefits include increased digestive efficiency [128][129][130][131][132], improved nitrogen economies achieved through the fixation or recycling of nitrogen [133][134][135], and the provisioning of essential, limiting nutrients like amino acids and B-vitamins [136][137][138].…”

Section: Symbiont Function and Implications For Variable Symbioses Within Coloniesmentioning

confidence: 99%

The secrets to domestic bliss – Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

D’Amelio

Béchade

et al. 2021

Preprint

Self Cite

View full text Add to dashboard Cite

Background: Gut microbiomes can vary across development, a pattern often found for insects with complete metamorphosis. With varying nutritional need and distinct opportunities for microbial acquisition, questions arise as to how such holometabolous insects retain helpful microbes at larval and adult stages. Ants are an intriguing system for such study. In a number of lineages adults digest only liquid food sources, while larvae digest solid foods. Like some other social insects, workers and soldiers of some ant species engage in oral-anal trophallaxes, enabling microbial transfer among siblings. But do queens, the typical colony founding caste, obtain symbionts through such transfer? Does this enable transgenerational symbiont passage? And does the resulting partner fidelity promote the evolution of beneficial symbionts? Furthermore, how might such adult-centric biology shape larval microbiomes? To address these questions, we characterized symbiotic gut bacteria across 13 species of Cephalotes turtle ants, with up to 40-million years of divergence. Adding to the prior focus on workers we, here, study underexplored castes and stages including queens, soldiers, and larvae, by performing 16S rRNA qPCR, amplicon sequencing, and phylogenetic classification. Results: We show that adult microbiomes are conserved across species and largely across castes. Nearly 95% of the bacteria in adults have, thus far, been found only in Cephalotes ants. Furthermore, the microbiomes from most adults exhibit phylosymbiosis, a trend in which microbiome community similarity recapitulates patterns of host relatedness. Additionally, an abundant, adult-enriched symbiont cospeciates with some Cephalotes. Evidence here suggests that these partner fidelity patterns extend from transgenerational symbiont transfer through alate gyne dispersal and subsequent colony-founding by queens. Like adults, larvae of Cephalotes species exhibit strong microbiome conservation. Phylosymbiosis patterns are weaker, however, with further evidence elevating environmental filtering as a primary mechanism behind such conservation. Specifically, while adult-enriched symbionts are found in most larvae, symbionts of older larvae are highly related to free-living bacteria from the Enterobacteriaceae, Lactobacillales, and Actinobacteria. Conclusions: Our findings suggest that both partner fidelity and conserved environmental filtering drive stable, stage-specific, social insect symbioses. We discuss the implications for our broader understanding of insect microbiomes, and the means of sustaining a beneficial microbiome.

show abstract

“…Chewing insects that feed on leaves would not have enough nitrogen solely from their diet. This insufficient nitrogen obtained from the diet would be supplemented by bacterial symbionts which can fix nitrogen and convert it into appropriate nitrogen-containing compounds (13,20,21). Some symbiotic bacteria could also protect the host against pathogens.…”

Section: Introductionmentioning

confidence: 99%

16S rRNA Amplicon Sequencing of BagwormMetisa planaWalker (Lepidoptera: Psychidae)

Ting

Abidin

Hamid

et al. 2021

Preprint

View full text Add to dashboard Cite

The bagworm Metisa plana is one of the major pests in the oil palm plantation in Malaysia, with infestation that results in huge economical loss. Currently, the exact cause of the infestation is still undetermined. Studying the bacterial community of M. plana could provide insight on the problem as the bacteria associated with insects often provide numerous benefits to the insect itself. Using 16S rRNA amplicon sequencing, the study was conducted to compare the composition of the bacterial communities of two larval stages (early instar stage and late instar stage) from outbreak area, as well as comparing the late instar stage larvae from non-outbreak and outbreak areas. Generally, the bacterial community was dominated by Proteobacteria and Actinobacteria phyla while the Enterobacteriaceae was found to be the dominant family. When comparing between the early and late instar stage, Proteobacteria phylum was found to be more abundant in the late instar stage (82.36%) than in the early instar stage (82.28%). At the family level, the Enterobacteriaceae was slightly more abundant in late instar stage (75.46%) than in early instar stage (75.29%). The instar stage was observed to have no significant impact on the bacterial variability and showed similar bacterial community structure. When comparing between the non-outbreak area and outbreak, Proteobacteria was significantly more abundant in the outbreak area (82.02%) than in the non-outbreak area (20.57%). However, Actinobacteria was significantly more abundant in the non-outbreak area (76.29%) than in the outbreak area (14.16%). At the family level, Enterobacteriaceae was more abundant in outbreak area (75.41%) than in non-outbreak area (11.67%). Microbacteriaceae was observed to be more abundant in the non-outbreak area (70.87%) than in the outbreak area (12.47%). Although the result showed no significant difference in bacterial variability between different areas, it the bacterial community structure was significantly different.

show abstract

Symbiotic solutions to nitrogen limitation and amino acid imbalance in insect diets

Cited by 34 publications

References 179 publications

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

In their sister’s footsteps: Taxonomic divergence obscures substantial functional overlap among the metabolically diverse symbiotic gut communities of adult and larval turtle ants

The secrets to domestic bliss – Partner fidelity and environmental filtering preserve stage-specific turtle ant gut symbioses for over 40 million years

16S rRNA Amplicon Sequencing of BagwormMetisa planaWalker (Lepidoptera: Psychidae)

Contact Info

Product

Resources

About