Ambrosia gall midges (AGMs) represent an intriguing group within the Cecidomyiidae, one of the most diversified dipteran families. AGMs form galls on plants, where they cultivate and consume fungal symbionts (phytomycetophagy). This mutualistic relationship may play a critical role in larval nutrition, gall morphogenesis, and protection against natural enemies. Although most other fungus-farming taxa have been intensively studied, AGMs have largely been neglected. This review synthesizes current knowledge on the diversity, biology, and ecological interactions of AGM, highlighting the intricate relationships with their fungal symbionts. The implications for adaptive radiation and speciation are critically considered, including how fungal associations may have facilitated ecological flexibility and diversification. We also tackle the processes of coevolution, not only between AGM and their fungal symbionts but also involving plants and parasitoids. We identify the most pressing issues and discrepancies in the current understanding the AGM-fungi interactions. Key areas of future research should include elucidating fungal acquisition and transmission mechanisms, determining the specificity and diversity of AGM-associated fungal communities, understanding the evolutionary pathways leading to phytomycetophagy, and addressing taxonomic challenges within the AGM group, where species identification has been complicated by reliance on gall morphology and host specificity.
- Keywords
- ambrosia gall midges, fungal symbionts, fungus farming, host shift, host specialization, phytomycetophagy,
- MeSH
- Biological Evolution * MeSH
- Diptera * microbiology physiology MeSH
- Fungi * physiology MeSH
- Plant Tumors parasitology MeSH
- Symbiosis * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Review MeSH
The bacterial genus Sodalis is represented by insect endosymbionts as well as free-living species. While the former have been studied frequently, the distribution of the latter is not yet clear. Here, we present a description of a free-living strain, Sodalis ligni sp. nov., originating from decomposing deadwood. The favored occurrence of S. ligni in deadwood is confirmed by both 16S rRNA gene distribution and metagenome data. Pangenome analysis of available Sodalis genomes shows at least three groups within the Sodalis genus: deadwood-associated strains, tsetse fly endosymbionts and endosymbionts of other insects. This differentiation is consistent in terms of the gene frequency level, genome similarity and carbohydrate-active enzyme composition of the genomes. Deadwood-associated strains contain genes for active decomposition of biopolymers of plant and fungal origin and can utilize more diverse carbon sources than their symbiotic relatives. Deadwood-associated strains, but not other Sodalis strains, have the genetic potential to fix N2, and the corresponding genes are expressed in deadwood. Nitrogenase genes are located within the genomes of Sodalis, including S. ligni, at multiple loci represented by more gene variants. We show decomposing wood to be a previously undescribed habitat of the genus Sodalis that appears to show striking ecological divergence.
- Keywords
- Sodalis, deadwood, free-living, insect symbionts, nitrogen fixation, non-symbiotic,
- Publication type
- Journal Article MeSH
Microbial symbionts commonly protect their hosts from natural enemies, but it is unclear how protective symbionts influence the evolution of host immunity to pathogens. One possibility is that 'extrinsic' protection provided by symbionts allows hosts to reduce investment in 'intrinsic' immunological resistance mechanisms. We tested this idea using pea aphids (Acyrthosiphon pisum) and their facultative bacterial symbionts that increase host resistance to the fungal pathogen Pandora neoaphidis. The pea aphid taxon is composed of multiple host plant associated populations called biotypes, which harbor characteristic communities of symbionts. We found that biotypes that more frequently carry protective symbionts have higher, rather than lower, levels of intrinsic resistance. Within a biotype there was no difference in intrinsic resistance between clones that did and did not carry a protective symbiont. The host plant on which an aphid feeds did not strongly influence intrinsic resistance. We describe a simple conceptual model of the interaction between intrinsic and extrinsic resistance and suggest that our results may be explained by selection favoring both the acquisition of protective symbionts and enhanced intrinsic resistance in habitats with high pathogen pressure. Such combined protection is potentially more robust than intrinsic resistance alone.
- Keywords
- ecological immunology, resistance, robustness, symbiosis,
- Publication type
- Journal Article MeSH
The association between anaerobic ciliates and methanogenic archaea has been recognized for over a century. Nevertheless, knowledge of these associations is limited to a few ciliate species, and so the identification of patterns of host-symbiont specificity has been largely speculative. In this study, we integrated microscopy and genetic identification to survey the methanogenic symbionts of 32 free-living anaerobic ciliate species, mainly from the order Metopida. Based on Sanger and Illumina sequencing of the 16S rRNA gene, our results show that a single methanogenic symbiont population, belonging to Methanobacterium, Methanoregula, or Methanocorpusculum, is dominant in each host strain. Moreover, the host's taxonomy (genus and above) and environment (i.e. endobiotic, marine/brackish, or freshwater) are linked with the methanogen identity at the genus level, demonstrating a strong specificity and fidelity in the association. We also established cultures containing artificially co-occurring anaerobic ciliate species harboring different methanogenic symbionts. This revealed that the host-methanogen relationship is stable over short timescales in cultures without evidence of methanogenic symbiont exchanges, although our intraspecific survey indicated that metopids also tend to replace their methanogens over longer evolutionary timescales. Therefore, anaerobic ciliates have adapted a mixed transmission mode to maintain and replace their methanogenic symbionts, allowing them to thrive in oxygen-depleted environments.
- Keywords
- anaerobiosis, archaea, endosymbionts, methane, symbiosis, syntrophy, transmission mode,
- MeSH
- Anaerobiosis MeSH
- Ciliophora * classification genetics physiology MeSH
- DNA, Archaeal genetics MeSH
- Ecosystem * MeSH
- Phylogeny * MeSH
- Methane * metabolism MeSH
- RNA, Ribosomal, 16S * genetics MeSH
- Sequence Analysis, DNA MeSH
- Symbiosis * MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- DNA, Archaeal MeSH
- Methane * MeSH
- RNA, Ribosomal, 16S * MeSH
Eukaryotes commonly host communities of heritable symbiotic bacteria, many of which are not essential for their hosts' survival and reproduction. There is laboratory evidence that these facultative symbionts can provide useful adaptations, such as increased resistance to natural enemies. However, we do not know how symbionts affect host fitness when the latter are subject to attack by a natural suite of parasites and pathogens. Here, we test whether two protective symbionts, Regiella insecticola and Hamiltonella defensa, increase the fitness of their host, the pea aphid (Acyrthosiphon pisum), under natural conditions. We placed experimental populations of two pea aphid lines, each with and without symbionts, in five wet meadow sites to expose them to a natural assembly of enemy species. The aphids were then retrieved and mortality from parasitoids, fungal pathogens and other causes assessed. We found that both Regiella and Hamiltonella reduce the proportion of aphids killed by the specific natural enemies against which they have been shown to protect in laboratory and cage experiments. However, this advantage was nullified (Hamiltonella) or reversed (Regiella) by an increase in mortality from other natural enemies and by the cost of carrying the symbiont. Symbionts therefore affect community structure by altering the relative success of different natural enemies. Our results show that protective symbionts are not necessarily advantageous to their hosts, and may even behave more like parasites than mutualists. Nevertheless, bacterial symbionts may play an important role in determining food web structure and dynamics.
- Keywords
- aphid *, field experiment *, host-parasite *, host-pathogen *, interactions *, symbiosis *,
- MeSH
- Enterobacteriaceae physiology MeSH
- Genetic Fitness MeSH
- Fungi physiology MeSH
- Host-Parasite Interactions MeSH
- Host-Pathogen Interactions * MeSH
- Aphids genetics microbiology parasitology physiology MeSH
- Wasps physiology MeSH
- Symbiosis * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
Only a few insect species are known to engage in symbiotic associations with antibiotic-producing Actinobacteria and profit from this kind of protection against pathogens. However, it still remains elusive how widespread the symbiotic interactions with Actinobacteria in other organisms are and how these partnerships benefit the hosts in terms of the growth and survival. We characterized a drastic temperature-induced change in the occurrence of Actinobacteria in the gut of the terrestrial isopod Porcellio scaber reared under two different temperature (15 °C and 22 °C) and oxygen conditions (10% and 22% O2) using 16S rRNA gene sequencing. We show that the relative abundance of actinobacterial gut symbionts correlates with increased host growth at lower temperature. Actinobacterial symbionts were almost completely absent at 22 °C under both high and low oxygen conditions. In addition, we identified members of nearly half of the known actinobacterial families in the isopod microbiome, and most of these include members that are known to produce antibiotics. Our study suggests that hosting diverse actinobacterial symbionts may provide conditions favorable for host growth. These findings show how a temperature-driven decline in microbiome diversity may cause a loss of beneficial functions with negative effects on ectotherms.
- Keywords
- Ambient temperature, Antibiotic-producing Actinobacteria, Gut microbiome, Holobiont, Host growth, Terrestrial isopod,
- MeSH
- Actinobacteria genetics physiology MeSH
- Isopoda microbiology physiology MeSH
- Oxygen metabolism MeSH
- RNA, Ribosomal, 16S genetics MeSH
- Symbiosis * MeSH
- Temperature MeSH
- Hot Temperature MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Oxygen MeSH
- RNA, Ribosomal, 16S MeSH
Bacterial endosymbionts evolve under strong host-driven selection. Factors influencing host evolution might affect symbionts in similar ways, potentially leading to correlations between the molecular evolutionary rates of hosts and symbionts. Although there is evidence of rate correlations between mitochondrial and nuclear genes, similar investigations of hosts and symbionts are lacking. Here, we demonstrate a correlation in molecular rates between the genomes of an endosymbiont (Blattabacterium cuenoti) and the mitochondrial genomes of their hosts (cockroaches). We used partial genome data for multiple strains of B. cuenoti to compare phylogenetic relationships and evolutionary rates for 55 cockroach/symbiont pairs. The phylogenies inferred for B. cuenoti and the mitochondrial genomes of their hosts were largely congruent, as expected from their identical maternal and cytoplasmic mode of inheritance. We found a correlation between evolutionary rates of the two genomes, based on comparisons of root-to-tip distances and on comparisons of the branch lengths of phylogenetically independent species pairs. Our results underscore the profound effects that long-term symbiosis can have on the biology of each symbiotic partner.
- Keywords
- Blattabacterium cuenoti, cockroach, host–symbiont interaction, molecular evolution, phylogeny, substitution rate,
- MeSH
- Phylogeny MeSH
- Genome, Bacterial MeSH
- Genome, Mitochondrial * MeSH
- Evolution, Molecular MeSH
- Cockroaches * MeSH
- Symbiosis MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
The research on anaerobic ciliates, to date, has mainly been focused on representatives of obligately anaerobic classes such as Armophorea or Plagiopylea. In this study, we focus on the anaerobic representatives of the subclass Scuticociliatia, members of the class Oligohymenophorea, which is mainly composed of aerobic ciliates. Until now, only a single anaerobic species, Cyclidium porcatum (here transferred to the genus Anaerocyclidium gen. nov.), has been described both molecularly and morphologically. Our broad sampling of anoxic sediments together with cultivation and single cell sequencing approaches have shown that scuticociliates are common and diversified in anoxic environments. Our results show that anaerobic scuticociliates represent a distinctive evolutionary lineage not closely related to the family Cyclidiidae (order Pleuronematida), as previously suggested. However, the phylogenetic position of the newly recognized lineage within the subclass Scuticociliatia remains unresolved. Based on molecular and morphological data, we establish the family Anaerocyclidiidae fam. nov. to accommodate members of this clade. We further provide detailed morphological descriptions and 18S rRNA gene sequences for six new Anaerocyclidium species and significantly broaden the described diversity of anaerobic scuticociliates.
UNLABELLED: The intracellular parasite Cardinium influences the bacterial microbiome composition of arthropod hosts; however, the mechanisms involved remain poorly understood. We sought to evaluate the interactions between Cardinium (cTPut) and SOL in Tyrophagus putrescentiae cultures based on relative abundance and gene expression data. First, we assembled the genome of Candidatus Krakonobacterium acarorum (formerly the Soliltalea-like symbiont SOL), a novel lineage of the Bacteroidota symbiont of mites. The assemblage SOL genome (1.2 Mb) contained complete pathways for the biosynthesis of lipoic acids, pantothenate, and menaquinone from futalosine. SOL is considered a facultative inhabitant (with prevalences ranging from 36% to 80% among individuals) of the gut (from 102 to 104 copies/mite) that is not detected in eggs, suggesting an extracellular location in the gut of mites. Second, gene expression was analyzed in SOL-inhabited cultures, including two cultures with cTPut and two cultures without cTPut. Correlation-based evidence for competition between cTPut and SOL was found mainly in the expression of transporter proteins. The presence of cTPut decreased interactions between SOL and the mite host; however, SOL is under greater control by mites in the presence of cTPut than in the absence of cTPut. Mite KEGG gene expression levels in the peroxisome, autophagy, sphingolipid, apoptosis, PI3K-Akt, and lysozyme pathways were more strongly correlated with SOL gene expression in cultures without cTPut than in those with cTPut. In contrast, mite KEGG gene expression levels in the proteasome, NF-κB, TNF, calcium, and Rap1 signaling pathways were more strongly correlated with SOL in the presence of cTPut. The explanation for these results is that cTPut mostly interacts with the mite host, resulting in changes in the host's immunity-related/regulatory pathways, indirectly affecting the symbiont SOL. IMPORTANCE: Here, we describe the novel Bacteroidetes symbiont (SOL) of mites. The analysis of gene expression in meta-transcriptomic samples from cultures with and without the intracellular parasite Cardinium revealed the effect of Cardinium on SOL as a model facultative symbiont of mites. Our findings suggest that there is competition between these two symbionts for nutrients. In addition, Cardinium can influence other bacterial symbionts via mite host immunity-related and regulatory pathways. Tyrophagus putrescentiae is a cosmopolitan pest mite that contaminates the home environment, including stored food and feed, with allergens. The interactions between intracellular bacteria and other members of the microbiome influence host physiology and indirectly affect allergen production.
- Keywords
- Bacteroidetes, Bacteroidota, Cardinium, gene expression, interaction, mite, symbionts,
- MeSH
- Acaridae * microbiology MeSH
- Bacteroidetes * genetics physiology classification MeSH
- Phylogeny MeSH
- Genome, Bacterial MeSH
- Mites * microbiology MeSH
- Gene Expression Profiling MeSH
- Symbiosis * MeSH
- Animals MeSH
- Check Tag
- Animals MeSH
- Publication type
- Journal Article MeSH
Amoebae play an important ecological role as predators in microbial communities. They also serve as niche for bacterial replication, harbor endosymbiotic bacteria and have contributed to the evolution of major human pathogens. Despite their high diversity, marine amoebae and their association with bacteria are poorly understood. Here we describe the isolation and characterization of two novel marine amoebae together with their bacterial endosymbionts, tentatively named 'Candidatus Occultobacter vannellae' and 'Candidatus Nucleophilum amoebae'. While one amoeba strain is related to Vannella, a genus common in marine habitats, the other represents a novel lineage in the Amoebozoa. The endosymbionts showed only low similarity to known bacteria (85-88% 16S rRNA sequence similarity) but together with other uncultured marine bacteria form a sister clade to the Coxiellaceae. Using fluorescence in situ hybridization and transmission electron microscopy, identity and intracellular location of both symbionts were confirmed; one was replicating in host-derived vacuoles, whereas the other was located in the perinuclear space of its amoeba host. This study sheds for the first time light on a so far neglected group of protists and their bacterial symbionts. The newly isolated strains represent easily maintainable model systems and pave the way for further studies on marine associations between amoebae and bacterial symbionts.
- MeSH
- Amoeba classification microbiology MeSH
- Cell Nucleus microbiology MeSH
- Cytoplasm microbiology MeSH
- Species Specificity MeSH
- Gammaproteobacteria classification isolation & purification physiology MeSH
- Symbiosis physiology MeSH
- Aquatic Organisms classification isolation & purification microbiology MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
