Coming together—symbiont acquisition and early development in deep-sea bathymodioline mussels

How and when symbionts are acquired by their animal hosts has a profound impact on the ecology and evolution of the symbiosis. Understanding symbiont acquisition is particularly challenging in deep-sea organisms because early life stages are so rarely found. Here, we collected early developmental stages of three deep-sea bathymodioline species from different habitats to identify when these acquire their symbionts and how their body plan adapts to a symbiotic lifestyle. These mussels gain their nutrition from chemosynthetic bacteria, allowing them to thrive at deep-sea vents and seeps worldwide. Correlative imaging analyses using synchrotron-radiation based microtomography together with light, fluorescence and electron microscopy revealed that the pediveliger larvae were aposymbiotic. Symbiont colonization began during metamorphosis from a planktonic to a benthic lifestyle, with the symbionts rapidly colonizing first the gills, the symbiotic organ of adults, followed by all other epithelia of their hosts. Once symbiont densities in plantigrades reached those of adults, the host's intestine changed from the looped anatomy typical for bivalves to a straightened form. Within the Mytilidae, this morphological change appears to be specific to Bathymodiolus and Gigantidas , and is probably linked to the decrease in the importance of filter feeding when these mussels switch to gaining their nutrition largely from their symbionts.

Inside or out? Clonal thiotrophic symbiont populations occupy deep-sea mussel bacteriocytes with pathways connecting to the external environment

Deep-sea Bathymodiolus mussels are generally thought to harbour chemosynthetic symbiotic bacteria in gill epithelial cells called bacteriocytes. However, previously observed openings at the apical surface of bacteriocytes have not been conclusively explained and investigated as to whether the Bathymodiolus symbiosis is intracellular or extracellular. In this study, we show that almost all the membranous chambers encompassing symbionts in a single bacteriocyte of Bathymodiolus septemdierum are interconnected and have pathways connecting to the external environment. Furthermore, the symbiont population colonising a single bacteriocyte is mostly clonal. This study hypothesises on a novel model of cellular localization at the interface between extra- and intracellular symbiosis, and the cellular-level process of symbiont acquisition in Bathymodiolus mussels.

Becoming symbiotic – the symbiont acquisition and the early development of bathymodiolin mussels

Symbiotic associations between animals and microorganisms are widespread and have a profound impact on the ecology, behaviour, physiology, and evolution of the host. Research on deep-sea mussels of the genus Bathymodiolus has revealed how chemosynthetic symbionts sustain their host with energy, allowing them to survive in the nutrient-poor environment of the deep ocean. However, to date, we know little about the initial symbiont colonization and how this is integrated into the early development of these mussels. Here we analysed the early developmental life stages of B. azoricus, “B”. childressi and B. puteoserpentis and the changes that occur once the mussels are colonized by symbionts. We combined synchrotron-radiation based μCT, correlative light and electron microscopy and fluorescence in situ hybridization to show that the symbiont colonization started when the animal settled on the sea floor and began its metamorphosis into an adult animal. Furthermore, we observed aposymbiotic life stages with a fully developed digestive system which was streamlined after symbiont acquisition. This suggests that bathymodiolin mussels change their nutritional strategy from initial filter-feeding to relying on the energy provided by their symbionts. After ~35 years of research on bathymodiolin mussels, we are beginning to answer fundamental ecological questions concerning their life cycle and the establishment of symbiosis.

Fish predation on corals promotes the dispersal of coral symbionts

Predators drive top-down effects that shape prey communities, but the role of predators in dispersing prey microbiomes is rarely examined. We tested whether coral-eating (corallivorous) fish disperse the single-celled dinoflagellate symbionts (family Symbiodiniaceae) of their prey. Our findings demonstrate that: (1) coral-eating fish egest feces containing live Symbiodiniaceae at densities up to seven orders of magnitude higher than other environmental reservoirs such as sediments and water; (2) Symbiodiniaceae communities in the feces of most corallivores are compositionally similar to those in corals; (3) some obligate corallivore species release over 100 million Symbiodiniaceae cells per 100 m2 per day; and (4) after being egested, corallivore feces often come in direct contact with coral colonies (potential hosts for Symbiodiniaceae). These findings suggest that fish predators can play an important role in symbiont acquisition by corals; such predators may have a previously unrecognized, indirect positive effect on prey health.

High temperature inhibits cnidarian-dinoflagellate symbiosis establishment through nitric oxide signaling

Coral reef ecosystems depend on a functional symbiosis between corals and photosynthetic dinoflagellate symbionts (Symbiodiniaceae), which reside inside the coral cells. Symbionts transfer nutrients essential for the corals’ survival, and loss of symbionts (‘coral bleaching’) can result in coral death. Temperature stress is one factor that can induce bleaching and is associated with the molecule nitric oxide (NO). Likewise, symbiont acquisition by aposymbiotic hosts is sensitive to elevated temperatures, but to date the role of NO signaling in symbiosis establishment is unknown. To address this, we use symbiosis establishment assays in aposymbiotic larvae of the anemone model Exaiptasia pallida (Aiptasia). We show that elevated temperature (32°C) enhances NO production in cultured symbionts but not in aposymbiotic larvae. Additionally, we find that symbiosis establishment is impaired at 32°C, and this same impairment is observed at control temperature (26°C) in the presence of a specific NO donor (GSNO). Conversely, the specific NO scavenger (cPTIO) restores symbiosis establishment at 32°C; however, reduction in NO levels at 26°C reduces the efficiency of symbiont acquisition. Our findings indicate that explicit NO levels are crucial for symbiosis establishment, highlighting the complexity of molecular signaling between partners and the adverse implications of temperature stress on coral reefs.

Pseudoscorpion Wolbachia symbionts: Diversity and Evidence for a New Supergroup S

Background Wolbachia are the most widely spread endosymbiotic bacteria, present in a wide variety of insects and two families of nematodes, but as of now, relatively little genomic data has been available. The Wolbachia symbiont can be parasitic, as described for many arthropod systems, an obligate mutualist, as in filarial nematodes or a combination of both in some organisms. They are currently classified into 16 monophyletic lineage groups ("supergroups"). Although the nature of these symbioses remains largely unknown, expanded Wolbachia genomic data will contribute to understanding their diverse symbiotic mechanisms and evolution. Results This report focuses on Wolbachia infections in three pseudoscorpion species infected by two distinct groups of Wolbachia strains , based upon multi-locus phylogenies. Geogarypus minor harbours w Gmin and Chthonius ischnocheles harbours w Cisc, both closely related to supergroup H, while Atemnus politus harbours w Apol, a member of a novel supergroup S along with Wolbachia from the pseudoscorpion Cordylochernes scorpioides ( w Csco), most closely related to Wolbachia supergroups C and F. Using target enrichment by hybridization with Wolbachia -specific biotinylated probes to capture large fragments of Wolbachia DNA, we produced two draft genomes of w Apol. Annotation of w Apol highlights presence of a biotin operon, which is incomplete in many sequenced Wolbachia genomes. Conclusions The present study highlights at least two symbiont acquisition events among pseudoscorpion species. Phylogenomic analysis indicates that the Wolbachia from Atemnus politus ( w Apol), forms a separate supergroup ("S") with the Wolbachia from Cordylochernes scorpioides (w Csco). Interestingly, the biotin operon, present in w Apol, appears to have been horizontally transferred multiple times along Wolbachia evolutionary history.

Pseudoscorpion Wolbachia symbionts: Diversity and Evidence for a New Supergroup S

Background Wolbachia are the most widely spread endosymbiotic bacteria, present in a wide variety of insects and two families of nematodes, but as of now, relatively little genomic data has been available. The Wolbachia symbiont can be parasitic, as described for many arthropod systems, an obligate mutualist, as in filarial nematodes or a combination of both in some organisms. They are currently classified into 16 monophyletic lineage groups ("supergroups"). Although the nature of these symbioses remains largely unknown, expanded Wolbachia genomic data will contribute to understanding their diverse symbiotic mechanisms and evolution. Results This report focuses on Wolbachia infections in three pseudoscorpion species infected by two distinct groups of Wolbachia strains , based upon multi-locus phylogenies. Geogarypus minor harbours w Gmin and Chthonius ischnocheles harbours w Cisc, both closely related to supergroup H, while Atemnus politus harbours w Apol, a member of a novel supergroup S along with Wolbachia from the pseudoscorpion Cordylochernes scorpioides ( w Csco), most closely related to Wolbachia supergroups C and F. Using target enrichment by hybridization with Wolbachia -specific biotinylated probes to capture large fragments of Wolbachia DNA, we produced two draft genomes of w Apol. Annotation of w Apol highlights presence of a biotin operon, which is incomplete in many sequenced Wolbachia genomes. Conclusions The present study highlights at least two symbiont acquisition events among pseudoscorpion species. Phylogenomic analysis indicates that the Wolbachia from Atemnus politus ( w Apol), forms a separate supergroup ("S") with the Wolbachia from Cordylochernes scorpioides (w Csco). Interestingly, the biotin operon, present in w Apol, appears to have been horizontally transferred multiple times along Wolbachia evolutionary history.

Versatile and Dynamic Symbioses Between Insects and Burkholderia Bacteria

Symbiotic associations with microorganisms represent major sources of ecological and evolutionary innovations in insects. Multiple insect taxa engage in symbioses with bacteria of the genus Burkholderia, a diverse group that is widespread across different environments and whose members can be mutualistic or pathogenic to plants, fungi, and animals. Burkholderia symbionts provide nutritional benefits and resistance against insecticides to stinkbugs, defend Lagria beetle eggs against pathogenic fungi, and may be involved in nitrogen metabolism in ants. In contrast to many other insect symbioses, the known associations with Burkholderia are characterized by environmental symbiont acquisition or mixed-mode transmission, resulting in interesting ecological and evolutionary dynamics of symbiont strain composition. Insect– Burkholderia symbioses present valuable model systems from which to derive insights into general principles governing symbiotic interactions because they are often experimentally and genetically tractable and span a large fraction of the diversity of functions, localizations, and transmission routes represented in insect symbioses.

A new symbiotic lineage related to Neisseria and Snodgrassella arises from the dynamic and diverse microbiomes in sucking lice

Phylogenetic diversity of symbiotic bacteria in sucking lice suggests that lice have experienced a complex history of symbiont acquisition, loss, and replacement during their evolution. By combining metagenomics and amplicon screening across several populations of two louse genera (Polyplax and Hoplopleura) we describe a novel louse symbiont lineage related to Neisseria and Snodgrassella, and show its’ independent origin within dynamic lice microbiomes. While the genomes of these symbionts are highly similar in both lice genera, their respective distributions and status within lice microbiomes indicate that they have different functions and history. In Hoplopleura acanthopus, the Neisseria-related bacterium is a dominant obligate symbiont universally present across several host’s populations, and seems to be replacing a presumably older and more degenerated obligate symbiont. In contrast, the Polyplax microbiomes are dominated by the obligate symbiont Legionella polyplacis, with the Neisseria-related bacterium co-occurring only in some samples and with much lower abundance.