Insight into the symbiotic lifestyle of DPANN archaea revealed by cultivation and genome analyses

Decades of culture-independent analyses have resulted in proposals of many tentative archaeal phyla with no cultivable representative. Members of DPANN (an acronym of the names of the first included phyla Diapherotrites, Parvarchaeota, Aenigmarchaeota, Nanohaloarchaeota, and Nanoarchaeota), an archaeal superphylum composed of at least 10 of these tentative phyla, are generally considered obligate symbionts dependent on other microorganisms. While many draft/complete genome sequences of DPANN archaea are available and their biological functions have been considerably predicted, only a few examples of their successful laboratory cultivation have been reported, limiting our knowledge of their symbiotic lifestyles. Here, we investigated physiology, morphology, and host specificity of an archaeon of the phylum “Candidatus Micrarchaeota” (ARM-1) belonging to the DPANN superphylum by cultivation. We constructed a stable coculture system composed of ARM-1 and its original host Metallosphaera sp. AS-7 belonging to the order Sulfolobales. Further host-switching experiments confirmed that ARM-1 grew on five different archaeal species from three genera—Metallosphaera, Acidianus, and Saccharolobus—originating from geologically distinct hot, acidic environments. The results suggested the existence of DPANN archaea that can grow by relying on a range of hosts. Genomic analyses showed inferred metabolic capabilities, common/unique genetic contents of ARM-1 among cultivated micrarchaeal representatives, and the possibility of horizontal gene transfer between ARM-1 and members of the order Sulfolobales. Our report sheds light on the symbiotic lifestyles of DPANN archaea and will contribute to the elucidation of their biological/ecological functions.

Odontonia kerangcaris sp. nov., a new bivalve-associated shrimp (Crustacea, Decapoda, Palaemonidae) from East Kalimantan, revealing intrageneric host switching

A new species of bivalve mollusk dwelling palaemonid shrimp of the genus Odontonia is described from the Berau Islands, East Kalimantan, Indonesia. This is the only Odontonia species recorded as a symbiont of a bivalve mollusk, all other congeners are known to associate with solitary ascidians. The new species belongs to the group wherein the dactylus of the ambulatory pereiopods has an accessory tooth. It differs from these species in the absence of a forward directed proximal tooth on the flexor margin of the corpus of the ambulatory dactyli. It also lacks the small denticles posterior to the distoventral accessory tooth on the dactylar corpus.

Effect of host-switching on the eco-evolutionary patterns of parasites

Increasing empirical evidence has revealed that host-switching is more common than cospeciation in the history of parasites. Here, we investigated how the intensity of host-switching, mediated by opportunity and compatibility, affects the phylogenetic history and ecology of the parasites. We developed a theoretical model to simulate the evolution of populations of parasites that can explore and colonize new hosts under variable host-switching intensities. Eco-evolutionary patterns (beta diversity/normalized Sackin index) obtained from parasite simulations were compared to nine empirical cases. Our model reproduced the empirical patterns, and such simulations varied in host-switching intensity according to the analysed case. This intensity does not differ among cases of ecto and endoparasites, but it was stronger in local cases when compared to a regional scale. Our results highlight the importance of contact opportunity, and suggest that host-switching intensity mediates the exploration and colonization of new hosts promoting variation in the eco-evolutionary patterns. Key-words: dispersion of parasites, opportunity and compatibility of interaction, phylogenetic conservatism and structure of community of parasites.

SARS-CoV-2 evolution in animals suggests mechanisms for rapid variant selection

SARS-CoV-2 spillback from humans into domestic and wild animals has been well documented, and an accumulating number of studies illustrate that human-to-animal transmission is widespread in cats, mink, deer, and other species. Experimental inoculations of cats, mink, and ferrets have perpetuated transmission cycles. We sequenced full genomes of Vero cell–expanded SARS-CoV-2 inoculum and viruses recovered from cats (n = 6), dogs (n = 3), hamsters (n = 3), and a ferret (n = 1) following experimental exposure. Five nonsynonymous changes relative to the USA-WA1/2020 prototype strain were near fixation in the stock used for inoculation but had reverted to wild-type sequences at these sites in dogs, cats, and hamsters within 1- to 3-d postexposure. A total of 14 emergent variants (six in nonstructural genes, six in spike, and one each in orf8 and nucleocapsid) were detected in viruses recovered from animals. This included substitutions in spike residues H69, N501, and D614, which also vary in human lineages of concern. Even though a live virus was not cultured from dogs, substitutions in replicase genes were detected in amplified sequences. The rapid selection of SARS-CoV-2 variants in vitro and in vivo reveals residues with functional significance during host switching. These observations also illustrate the potential for spillback from animal hosts to accelerate the evolution of new viral lineages, findings of particular concern for dogs and cats living in households with COVID-19 patients. More generally, this glimpse into viral host switching reveals the unrealized rapidity and plasticity of viral evolution in experimental animal model systems.

Effect of host switching simulation on the fitness of the gregarious parasitoid Anaphes flavipes from a novel two-generation approach

Herbivorous insects can escape the strong pressure of parasitoids by switching to feeding on new host plants. Parasitoids can adapt to this change but at the cost of changing their preferences and performance. For gregarious parasitoids, fitness changes are not always observable in the F1 generation but only in the F2 generation. Here, with the model species and gregarious parasitoid Anaphes flavipes, we examined fitness changes in the F1 generation under pressure from the simulation of host switching, and by a new two-generation approach, we determined the impact of these changes on fitness in the F2 generation. We showed that the parasitoid preference for host plants depends on hatched or oviposited learning in relation to the possibility of parasitoid decisions between different host plants. Interestingly, we showed that after simulation of parasitoids following host switching, in the new environment of a fictitious host plant, parasitoids reduced the fictitious host. At the same time, parasitoids also reduced fertility because in fictitious hosts, they are not able to complete larval development. However, from a two-generation approach, the distribution of parasitoid offspring into both native and fictitious hosts caused lower parasitoid clutch size in native hosts and higher individual offspring fertility in the F2 generation.

The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range

Host switching allows parasites to expand their niches. However, successful switching may require suites of adaptations and also may decrease performance on the old host. As a result, reductions in gene flow accompany many host switches, driving speciation. Because host switches tend to be rapid, it is difficult to study their demographic parameters in real-time. Fundamental factors that control subsequent parasite evolution, such as the size of the switching population or the extent of immigration from the original host, remain largely unknown. To shed light on the host switching process, we explored the history of independent switches by two ectoparasitic honey bee mites (Varroa destructor and V. jacobsoni). Both switched to the western honey bee (Apis mellifera) after it was brought into contact with their ancestral host (Apis cerana), ~70 and ~12 years ago, respectively. Varroa destructor subsequently caused worldwide collapses of honey bee populations. Using whole-genome sequencing on 63 mites collected in their native ranges from both the ancestral and novel hosts, we were able to reconstruct the known temporal dynamics of the switch. We further found multiple previously undiscovered mitochondrial lineages on the novel host, along with the genetic equivalent of tens of individuals that were involved in the initial host switch. Despite being greatly reduced, some gene flow remains between mites adapted to different hosts. Our findings suggest that while reproductive isolation may facilitate the fixation of traits beneficial for exploitation of the new host, ongoing genetic exchange may allow genetic amelioration of inbreeding effects.

Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites

Adaptive radiation is an important mechanism of organismal diversification, and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites present an ideal system to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have undergone an adaptive radiation, resulting in differences in both body size and overall coloration. Here we show that long-distance dispersal by dove hosts was important for parasite diversification, providing new ecological opportunities for parasites to speciate by host-switching. We further show that these new opportunities for host-switching decreased over time, and cospeciation became the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.