Microbiome Changes of Endemic Lake Baikal Sponges during Bleaching Syndrome Development

The sponge (Porifera) microbiome is an indicator of both natural and anthropogenic stressors. Studying Baikal sponge microbial communities could help reveal if there is a connection between bacterial symbionts and a mass sponge bleaching event that was recently detected; 16S rRNA sequencing was performed among healthy and diseased freshwater sponges of Lubomirskia baikalensis and Baikalospongia intermedia, which were collected from Lake Baikal, Russia. A phylum-based taxonomic classification showed that Chlorophyta, Acidobacteria, Bacteroidetes, Actinobacteria and Cyanobacteria were most abundant across samples. When comparing healthy and diseased L. baikalensis samples, large variations in microbial composition were found at the phylum level. Comparative analyses, which were performed for the first time for B. intermedia, showed a decrease in Chlorophyta (unicellular green algae) and an increase in Bacteroidetes and Cyanobacteria in diseased specimens. At the genus level, the Opitutus (Verrucomicrobia), Planctomyces, and Nitrospira content increased in all diseased sponges, which reflected a general tendency toward an increase in Cyanobacteria in diseased sponges. Comparative analysis of the diseased and healthy sponge metagenomes showed that diseased sponges underwent various nonspecific changes in bacterial composition. The bacterial community composition is probably influenced by sponge type and degree of disease affection.

Ploidy dynamics in aphid host cells harboring bacterial symbionts

Aphids have evolved bacteriocytes or symbiotic host cells that harbor the obligate mutualistic bacterium Buchnera aphidicola. Because of the large cell size (approximately 100 μm in diameter) of bacteriocytes and their pivotal role in nutritional symbiosis, researchers have considered that these cells are highly polyploid and assumed that bacteriocyte polyploidy may be essential for the symbiotic relationship between the aphid and the bacterium. However, little is known about the ploidy levels and dynamics of aphid bacteriocytes. Here, we quantitatively analyzed the ploidy levels in the bacteriocytes of the pea-aphid Acyrthosiphon pisum. Image-based fluorometry revealed the hyper polyploidy of the bacteriocytes ranging from 16- to 256-ploidy throughout the lifecycle. Bacteriocytes of adult parthenogenetic viviparous females were mainly 64-128C DNA levels, while those of sexual morphs (oviparous females and males) were consisted of 64C, and 32-64C cells, respectively. During post-embryonic development of viviparous females, the ploidy level of bacteriocytes increased substantially, from 16-32C at birth to 128-256C in actively reproducing adults. These results suggest that the ploidy levels are dynamically regulated among phenotypes and during development. Our comprehensive and quantitative data provides a foundation for future studies to understand the functional roles and biological significance of the polyploidy of insect bacteriocytes.

Microbiomes of Blood-Feeding Arthropods: Genes Coding for Essential Nutrients and Relation to Vector Fitness and Pathogenic Infections. A Review

Background: Blood-feeding arthropods support a diverse array of symbiotic microbes, some of which facilitate host growth and development whereas others are detrimental to vector-borne pathogens. We found a common core constituency among the microbiota of 16 different arthropod blood-sucking disease vectors, including Bacillaceae, Rickettsiaceae, Anaplasmataceae, Sphingomonadaceae, Enterobacteriaceae, Pseudomonadaceae, Moraxellaceae and Staphylococcaceae. By comparing 21 genomes of common bacterial symbionts in blood-feeding vectors versus non-blooding insects, we found that certain enteric bacteria benefit their hosts by upregulating numerous genes coding for essential nutrients. Bacteria of blood-sucking vectors expressed significantly more genes (p < 0.001) coding for these essential nutrients than those of non-blooding insects. Moreover, compared to endosymbionts, the genomes of enteric bacteria also contained significantly more genes (p < 0.001) that code for the synthesis of essential amino acids and proteins that detoxify reactive oxygen species. In contrast, microbes in non-blood-feeding insects expressed few gene families coding for these nutrient categories. We also discuss specific midgut bacteria essential for the normal development of pathogens (e.g., Leishmania) versus others that were detrimental (e.g., bacterial toxins in mosquitoes lethal to Plasmodium spp.).

Intracellular Bacterial Symbionts in Corals: Challenges and Future Directions

Corals are the main primary producers of coral reefs and build the three-dimensional reef structure that provides habitat to more than 25% of all marine eukaryotes. They harbor a complex consortium of microorganisms, including bacteria, archaea, fungi, viruses, and protists, which they rely on for their survival. The symbiosis between corals and bacteria is poorly studied, and their symbiotic relationships with intracellular bacteria are only just beginning to be acknowledged. In this review, we emphasize the importance of characterizing intracellular bacteria associated with corals and explore how successful approaches used to study such microorganisms in other systems could be adapted for research on corals. We propose a framework for the description, identification, and functional characterization of coral-associated intracellular bacterial symbionts. Finally, we highlight the possible value of intracellular bacteria in microbiome manipulation and mitigating coral bleaching.

A dual endosymbiosis drives nutritional adaptation to hematophagy in the invasive tick Hyalomma marginatum

Many animals are dependent on microbial partners that provide essential nutrients lacking from their diet. Ticks, whose diet consists exclusively on vertebrate blood, rely on maternally inherited bacterial symbionts to supply B vitamins. While previously studied tick species consistently harbor a single lineage of those nutritional symbionts, we evidence here that the invasive tick Hyalomma marginatum harbors a unique dual-partner nutritional system between an ancestral symbiont, Francisella, and a more recently acquired symbiont, Midichloria. Using metagenomics, we show that Francisella exhibits extensive genome erosion that endangers the nutritional symbiotic interactions: Its genome includes folate and riboflavin biosynthesis pathways but deprived functional biotin biosynthesis on account of massive pseudogenization. Co-symbiosis compensates this deficiency since the Midichloria genome encompasses an intact biotin operon, which was primarily acquired via lateral gene transfer from unrelated intracellular bacteria commonly infecting arthropods. Thus, in H. marginatum, a mosaic of co-evolved symbionts incorporating gene combinations of distant phylogenetic origins emerged to prevent the collapse of an ancestral nutritional symbiosis. Such dual endosymbiosis was never reported in other blood feeders but was recently documented in agricultural pests feeding on plant sap, suggesting that it may be a key mechanism for advanced adaptation of arthropods to specialized diets.

The Importance of Environmentally Acquired Bacterial Symbionts for the Squash Bug (Anasa tristis), a Significant Agricultural Pest

Most insects maintain associations with microbes that shape their ecology and evolution. Such symbioses have important applied implications when the associated insects are pests or vectors of disease. The squash bug, Anasa tristis (Coreoidea: Coreidae), is a significant pest of human agriculture in its own right and also causes damage to crops due to its capacity to transmit a bacterial plant pathogen. Here, we demonstrate that complete understanding of these insects requires consideration of their association with bacterial symbionts in the family Burkholderiaceae. Isolation and sequencing of bacteria housed in the insects’ midgut crypts indicates that these bacteria are consistent and dominant members of the crypt-associated bacterial communities. These symbionts are closely related to Caballeronia spp. associated with other true bugs in the superfamilies Lygaeoidea and Coreoidea. Fitness assays with representative Burkholderiaceae strains indicate that the association can significantly increase survival and decrease development time, though strains do vary in the benefits that they confer to their hosts, with Caballeronia spp. providing the greatest benefit. Experiments designed to assess transmission mode indicate that, unlike many other beneficial insect symbionts, the bacteria are not acquired from parents before or after hatching but are instead acquired from the environment after molting to a later developmental stage. The bacteria do, however, have the capacity to escape adults to be transmitted to later generations, leaving the possibility for a combination of indirect vertical and horizontal transmission.

Beetle–Bacterial Symbioses: Endless Forms Most Functional

Beetles are hosts to a remarkable diversity of bacterial symbionts. In this article, we review the role of these partnerships in promoting beetle fitness following a surge of recent studies characterizing symbiont localization and function across the Coleoptera. Symbiont contributions range from the supplementation of essential nutrients and digestive or detoxifying enzymes to the production of bioactive compounds providing defense against natural enemies. Insights on this functional diversity highlight how symbiosis can expand the host's ecological niche, but also constrain its evolutionary potential by promoting specialization. As bacterial localization can differ within and between beetle clades, we discuss how it corresponds to the microbe's beneficial role and outline the molecular and behavioral mechanisms underlying symbiont translocation and transmission by its holometabolous host. In reviewing this literature, we emphasize how the study of symbiosis can inform our understanding of the phenotypic innovations behind the evolutionary success of beetles. Expected final online publication date for the Annual Review of Entomology, Volume 67 is January 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

The Genetic Diversity of Rickettsiella Symbionts in Ixodes ricinus Throughout Europe

Rickettsiella species are bacterial symbionts that are present in a great variety of arthropod species, including ixodid ticks. However, little is known about their genetic diversity and distribution in Ixodes ricinus, as well as their relationship with other tick-associated bacteria. In this study, we investigated the occurrence and the genetic diversity of Rickettsiella spp. in I. ricinus throughout Europe and evaluated any preferential and antagonistic associations with Candidatus Midichloria mitochondrii and the pathogens Borrelia burgdorferi sensu lato and Borrelia miyamotoi. Rickettsiella spp. were detected in most I. ricinus populations investigated, encompassing a wide array of climate types and environments. The infection prevalence significantly differed between geographic locations and was significantly higher in adults than in immature life stages. Phylogenetic investigations and protein characterization disclosed four Rickettsiella clades (I–IV). Close phylogenetic relations were observed between Rickettsiella strains of I. ricinus and other arthropod species. Isolation patterns were detected for Clades II and IV, which were restricted to specific geographic areas. Lastly, although coinfections occurred, we did not detect significant associations between Rickettsiella spp. and the other tick-associated bacteria investigated. Our results suggest that Rickettsiella spp. are a genetically and biologically diverse facultative symbiont of I. ricinus and that their distribution among tick populations could be influenced by environmental components.

Transmission of Bacterial Symbionts With and Without Genome Erosion Between a Beetle Host and the Plant Environment

Many phytophagous insects harbor symbiotic bacteria that can be transmitted vertically from parents to offspring, or acquired horizontally from unrelated hosts or the environment. In the latter case, plants are a potential route for symbiont transfer and can thus foster a tripartite interaction between microbe, insect, and plant. Here, we focus on two bacterial symbionts of the darkling beetle Lagria villosa that belong to the genus Burkholderia; the culturable strain B. gladioli Lv-StA and the reduced-genome strain Burkholderia Lv-StB. The strains can be transmitted vertically and confer protection to the beetle’s eggs, but Lv-StA can also proliferate in plants, and both symbiont strains have presumably evolved from plant pathogens. Notably, little is known about the role of the environment for the transmission dynamics and the maintenance of the symbionts. Through manipulative assays, we demonstrate the transfer of the symbionts from the beetle to wheat, rice and soybean plants, as well as leaf litter. In addition, we confirm that aposymbiotic larvae can pick up Lv-StA from dry leaves and the symbiont can successfully establish in the beetle’s symbiotic organs. Also, we show that the presence of plants and soil in the environment improves symbiont maintenance. These results indicate that the symbionts of L. villosa beetles are still capable of interacting with plants despite signatures of genome erosion and suggest that a mixed-mode of bacterial transmission is likely key for the persistence of the symbiosis.