Variable organization of symbiont-containing tissue across planthoppers hosting different heritable endosymbionts

Frontiers in Physiology, Journal Year: 2023, Volume and Issue: 14

Published: March 22, 2023

Sap-feeding hemipteran insects live in associations with diverse heritable symbiotic microorganisms (bacteria and fungi) that provide essential nutrients deficient their hosts' diets. These symbionts typically reside highly specialized organs called bacteriomes (with bacterial symbionts) or mycetomes fungal symbionts). The organization of these varies between insect clades are ancestrally associated different microbes. As symbioses evolve additional complement replace the ancient associates, symbiont-containing tissue becomes even more variable. Planthoppers (Hemiptera: Fulgoromorpha) Sulcia Vidania, but many planthopper lineages, now accompanied have been replaced by other bacteria (e.g., Sodalis, Arsenophonus, Purcelliella) fungi. We know identity microbes, symbiont distribution within host tissues bacteriome not systematically studied using modern microscopy techniques. Here, we combine light, fluorescence, transmission electron phylogenomic data to compare distributions across planthoppers representing 15 families. identify describe seven primary types localization bacteriome. show when present, usually occupy distinct distributed body cavity. recently acquired gammaproteobacterial generally separate groups cells organized into mycetomes, from those Vidania. They can also be localized cytoplasm fat cells. Alphaproteobacterial colonize a wider range habitats: Asaia-like often gut lumen, whereas Wolbachia Rickettsia scattered cell types, including containing symbionts, sheath, cells, epithelium, as well hemolymph. However, there exceptions, Gammaproteobacteria share Alphaproteobacteria discuss how correlates acquisition replacement patterns symbionts' likely functions. evolutionary consequences, constraints, significance findings.

Language: Английский

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Diversity and genomics of bacteriome-associated symbionts in treehopper Darthula hardwickii (Hemiptera: Aetalionidae) and implications of their nutritional functions

Applied and Environmental Microbiology, Journal Year: 2025, Volume and Issue: unknown

Published: March 4, 2025

ABSTRACT Symbionts play important roles in insect nutritional ecology, and the phylogenies of some vertically transmitted symbionts mirror host phylogeny. Here we report diversity, distribution, transmission, potential functions harbored aetalionid treehopper Darthula hardwickii (Aetalionidae) using multiple methods compare its obligate symbiont Karelsulcia with that related Aetalion reticulatum. D. harbors bacteriomes, a yeast-like fungal (YLS) fat bodies, Tisiphia both bacteriomes bodies. YLS are to ovaries but do not cluster form “symbiont ball” terminal oocytes, as is case other auchenorrhynchan insects. represents first known instance being associated treehoppers. Phylogenetic analysis revealed Aetalionidae derived from within Membracidae. Gene truncation absence were tryptophan biosynthetic pathway , suggesting this no longer capable providing essential amino acid (EAA) host. Tryptophan presumed be supplied by since tryptophan-related genes either absent or degraded . No truncated found A. reticulatum it has lost synthesis EAAs, leafhoppers. This study sheds new light on diversity endosymbionts Membracoidea processes may have precipitated replacement diverse lineage. IMPORTANCE sap-feeding insects nutrition their hosts, which change through evolutionary time vary across lineages. comparative genomic indicates that, compared leaf- treehoppers, ability provide EAA function apparently performed coexisting (YLS). species treehopper, suggests involved treehoppers similar those observed sap-sucking analyses lineages largely phylogeny suggest originated Membracidae, contrast recent based data

Language: Английский

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Limited variation in microbial communities across populations of Macrosteles leafhoppers (Hemiptera: Cicadellidae)

Environmental Microbiology Reports, Journal Year: 2024, Volume and Issue: 16(3)

Published: June 1, 2024

Microbial symbionts play crucial roles in insect biology, yet their diversity, distribution, and temporal dynamics across host populations remain poorly understood. In this study, we investigated the spatio-temporal distribution of bacterial within widely distributed economically significant leafhopper genus Macrosteles, with a focus on Macrosteles laevis. Using symbiont marker gene amplicon sequencing, explored intricate relationships between these insects microbial partners. Our analysis cytochrome oxidase subunit I (COI) data revealed several intriguing findings. First, there was no strong genetic differentiation M. laevis populations, suggesting flow among them. Second, observed levels heteroplasmy, indicating presence multiple mitochondrial haplotypes individuals. Third, parasitoid infections were prevalent, highlighting complex ecological interactions involving leafhoppers. The 16S rRNA confirmed universal ancient nutritional endosymbionts-Sulcia Nasuia-in Additionally, found high prevalence Arsenophonus, another common symbiont. Interestingly, unlike most previously studied species, exhibited only occasional cases infection known facultative endosymbionts other bacteria. Notably, variation different or sampling years same population. Comparatively, such as Rickettsia, Wolbachia, Cardinium Lariskella more species. These findings underscore importance considering both when studying associations. By simultaneously characterizing amplicons large collections, gain valuable insights into interplay Understanding contributes to our broader comprehension host-microbe natural ecosystems.

Language: Английский

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Obligate mutualistic heritable symbiosis in sap-feeding insects: an intricate relationship in nature

Symbiosis, Journal Year: 2024, Volume and Issue: 92(2), P. 159 - 185

Published: Jan. 22, 2024

Language: Английский

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Endosymbioses Have Shaped the Evolution of Biological Diversity and Complexity Time and Time Again

Genome Biology and Evolution, Journal Year: 2024, Volume and Issue: 16(6)

Published: May 30, 2024

Abstract Life on Earth comprises prokaryotes and a broad assemblage of endosymbioses. The pages Molecular Biology Evolution Genome have provided an essential window into how these endosymbiotic interactions evolved shaped biological diversity. Here, we provide current perspective this knowledge by drawing decades revelatory research published in Evolution, insights from the field at large. accumulated work illustrates endosymbioses hosts with novel phenotypes that allow them to transition between adaptive landscapes access environmental resources. Such relationships reshaped life Earth. early serial establishment mitochondria chloroplasts through permitted massive upscaling cellular energetics, multicellularity, terrestrial planetary greening. These are also foundation upon which all later ones built, including everything land–plant fungi bacteria nutritional found invertebrate animals. Common evolutionary mechanisms range interactions. Endosymbionts generally experience stochastic genome streamlining, extent depends several key factors (e.g. mode transmission). Hosts, contrast, adapt complex resource exchange, integration regulation, genetic support prop up degraded symbionts. However, there significant differences not only partners each other but scope their influence important considerations for predicting will persist changing planet.

Language: Английский

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Distribution, Vertical Transmission, and Cooperative Mechanisms of Obligate Symbiotic Bacteria in the Leafhopper Maiestas dorsalis (Hemiptera, Cicadellidea)

Insects, Journal Year: 2023, Volume and Issue: 14(8), P. 710 - 710

Published: Aug. 14, 2023

Many insects rely on ancient symbiotic bacterial associations for essential nutrition. Auchenorrhyncha commonly harbor two obligate symbionts: Sulcia (Bacteroidetes) and a proteobacterial partner that supplies amino acids lacking in their plant-sap diets. In this study focusing Maiestas dorsalis, we investigated the distribution vertical transmission of bacteria, Nasuia, within leafhopper. primarily inhabits external region bacteriome, while Nasuia is restricted to internal region. Both symbionts progressively infiltrate ovary through epithelial plug, ultimately reaching developing primary oocyte. Furthermore, co-phylogenetic analysis suggests close correlation between evolution presence bacteria. Genomic further unveiled extreme genome reduction with retaining genes involved basic cellular processes limited energy synthesis, exhibited gene loss replication, transcription, translation, synthesis. However, both retained synthesizing required by host insect. Our highlights coevolutionary dynamics Sulcia, partners, insect hosts, shedding light intricate nutritional interactions evolutionary adaptations insects.

Language: Английский

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Limited variation in microbial communities across populations ofMacrostelesleafhoppers (Hemiptera: Cicadellidae)

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: Jan. 28, 2024

Summary Microbial symbionts play important roles in insect biology, but their diversity, distribution, and dynamics over time across host populations are poorly understood. We surveyed the spatio-temporal distribution of bacterial broadly distributed economically significant leafhopper genus Macrosteles , with emphasis on laevis using symbiont marker gene amplicon sequencing. The cytochrome oxidase I (COI) data revealed no strong genetic differentiation M. populations, levels heteroplasmy, multiple cases parasitoid infections. 16S rRNA confirmed universal presence ancient nutritional endosymbionts Sulcia Nasuia a high prevalence Arsenophonus . Interestingly, contrast to most previously species, we found only occasional infection facultative other bacteria. There was variation or among sampling years for same population. Facultative including Rickettsia Wolbachia Cardinium Lariskella were more common species. Combined, our demonstrate that not all species show clear spatial temporal structure microbial prevalence. However, simultaneous characterization amplicons large collections can help understand host-microbe interactions.

Language: Английский

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Facultatively intrabacterial localization of a planthopper endosymbiont as an adaptation to its vertical transmission

mSystems, Journal Year: 2024, Volume and Issue: 9(7)

Published: June 27, 2024

Transovarial transmission is the most reliable way of passing on essential nutrient-providing endosymbionts from mothers to offspring. However, not all endosymbiotic microbes follow complex path through female host tissues oocytes their own. Here, we demonstrate an unusual strategy adopted by one planthopper

Language: Английский

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Phylogenomics resolves the relationship and the evolutionary history of planthoppers (Insecta: Hemiptera: Fulgoromorpha)

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2024, Volume and Issue: unknown

Published: July 26, 2024

Abstract Planthoppers (Hemiptera: Fulgoromorpha) are a species-rich and globally distributed insect clade with high economic, ecological, evolutionary importance. However, the relationships among planthopper lineages families remain unclear. Previous efforts based on inconsistent morphological traits, few genes, or limited sampling often resulted in conflicting tree topologies. Here, we used genome-level data to assemble 1164 nuclear single-copy genes 13 mitochondrial protein-coding for 149 species representing 19 out of 21 extant families. Additional markers were added from published mitogenomes, expanding our 285 species. These Maximum Likelihood-based inference dating analyses. The newly inferred phylogenies validated well-accepted recovered novel placements. Taxonomic conclusions include establishment new family Borysthenidae stat. rev. within Delphacoidea superfamily Meenoploidea superfam. nov. including redefined Kinnaridae Meenoplidae , confirmation monophyletic Achilixiidae outside Achilidae-Derbidae clade, transfer tribes Lyncidini Amyclini Dictyopharidae genus Madagascaritia Fulgoridae. time analyses 57 30 fossils dated origin crown Fulgoromorpha back Guadalupian, Permian (∼263 Ma), close maximum constraint at 267.3 Ma, while applying an older root Mississippian, Carboniferous (∼332 Ma). While future unstudied fauna unexplored regions habitats may change topology, current phylogenomic analysis will serve as solid foundation research into ecology, evolution, significance.

Language: Английский

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Diversity and composition of the bacterial communities associated with the Australian spittlebugs Bathyllus albicinctus and Philagra parva (Hemiptera: Aphrophoridae)

PLoS ONE, Journal Year: 2024, Volume and Issue: 19(10), P. e0311938 - e0311938

Published: Oct. 10, 2024

Spittlebugs and froghoppers (Hemiptera: Cercopoidea) are insects feeding on xylem, which potentially can cause significant economic damage worldwide by transmitting plant pathogenic bacteria such as Xylella fastidiosa. Australia New Zealand currently free from X. fastidiosa, but they home to at least 45 native spittlebug species. Among these, the Australian natives Bathyllus albicinctus (Erichson, 1842) Philagra parva (Donovan, 1805) particularly widespread be found across southern eastern Australia, with B. also in Zealand. The potential that both species might capable of vectoring fastidiosa poses a substantial biosecurity risk if bacterium were invade these regions. In this study, we examined 87 nymphs collected 12 different host species, five locations Victoria, Australia. Our objective was explore factors influencing bacterial communities within between considering geographic location, insect phylogenetics, associations. We employed COI barcoding assess genetic variation 16S high throughput sequencing (HTS) metabarcoding analyse microbiome diversity various plants. findings revealed minimal divergence among individuals same highlighting conspecificity despite conspicuous morphological divergences. On other hand, recorded harboured plants, even when close proximity each other. Therefore, association appeared shape spittlebugs more than or geographical location. These diverse could facilitate transmission bacteria, underscoring numerous hosts through insect-plant interactions. This study emphasizes critical need understand complex interactions, context biosecurity.

Language: Английский

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