Ancient reindeer mitogenomes reveal island-hopping colonisation of the Arctic archipelagos.

Climate warming at the end of the last glacial period had profound effects on the distribution of cold-adapted species. As their range shifted towards northern latitudes, they were able to colonise previously glaciated areas, including remote Arctic islands. However, there is still uncertainty about the routes and timing of colonisation. At the end of the last ice age, reindeer/caribou (Rangifer tarandus) expanded to the Holarctic region and colonised the archipelagos of Svalbard and Franz Josef Land. Earlier studies have proposed two possible colonisation routes, either from the Eurasian mainland or from Canada via Greenland. Here, we used 174 ancient, historical and modern mitogenomes to reconstruct the phylogeny of reindeer across its whole range and to infer the colonisation route of the Arctic islands. Our data shows a close affinity among Svalbard, Franz Josef Land and Novaya Zemlya reindeer. We also found tentative evidence for positive selection in the mitochondrial gene ND4, which is possibly associated with increased heat production. Our results thus support a colonisation of the Eurasian Arctic archipelagos from the Eurasian mainland and provide some insights into the evolutionary history and adaptation of the species to its High Arctic habitat.

Host-gut microbiota interactions shape parasite infections in farmed Atlantic salmon.

Animals and their associated microbiota share long evolutionary histories. However, it is not always clear how host genotype and microbiota interact to affect phenotype. We applied a hologenomic approach to explore how host-microbiota interactions shape lifetime growth and parasite infection in farmed Atlantic salmon (Salmo salar). Multi-omics data sets were generated from the guts of 460 salmon, 82% of which were naturally infected with an intestinal cestode. A single Mycoplasma bacterial strain, MAG01, dominated the gut metagenome of large, non-parasitized fish, consistent with previous studies showing high levels of Mycoplasma in the gut microbiota of healthy salmon. While small and/or parasitized salmon also had high abundance of MAG01, we observed increased alpha diversity in these individuals, driven by increased frequency of low-abundance Vibrionaceae and other Mycoplasma species that carried known virulence genes. Colonization by one of these cestode-associated Mycoplasma strains was associated with host individual genomic variation in long non-coding RNAs. Integrating the multi-omic data sets revealed coordinated changes in the salmon gut mRNA transcriptome and metabolome that correlated with shifts in the microbiota of smaller, parasitized fish. Our results suggest that the gut microbiota of small and/or parasitized fish is in a state of dysbiosis that partly depends on the host genotype, highlighting the value of using a hologenomic approach to incorporate the microbiota into the study of host-parasite dynamics.IMPORTANCEStudying host-microbiota interactions through the perspective of the hologenome is gaining interest across all life sciences. Intestinal parasite infections are a huge burden on human and animal health; however, there are few studies investigating the role of the hologenome during parasite infections. We address this gap in the largest multi-omics fish microbiota study to date using natural cestode infection of farmed Atlantic salmon. We find a clear association between cestode infection, salmon lifetime growth, and perturbation of the salmon gut microbiota. Furthermore, we provide the first evidence that the genetic background of the host may partly determine how the gut microbiota changes during parasite-associated dysbiosis. Our study therefore highlights the value of a hologenomic approach for gaining a more in-depth understanding of parasitism.

Adaptation to the High-Arctic island environment despite long-term reduced genetic variation in Svalbard reindeer.

Typically much smaller in number than their mainland counterparts, island populations are ideal systems to investigate genetic threats to small populations. The Svalbard reindeer (Rangifer tarandus platyrhynchus) is an endemic subspecies that colonized the Svalbard archipelago ca. 6,000-8,000 years ago and now shows numerous physiological and morphological adaptations to its arctic habitat. Here, we report a de-novo chromosome-level assembly for Svalbard reindeer and analyze 133 reindeer genomes spanning Svalbard and most of the species' Holarctic range, to examine the genomic consequences of long-term isolation and small population size in this insular subspecies. Empirical data, demographic reconstructions, and forward simulations show that long-term isolation and high inbreeding levels may have facilitated the reduction of highly deleterious-and to a lesser extent, moderately deleterious-variation. Our study indicates that long-term reduced genetic diversity did not preclude local adaptation to the High Arctic, suggesting that even severely bottlenecked populations can retain evolutionary potential.

Co-diversification of an intestinal Mycoplasma and its salmonid host.

Understanding the evolutionary relationships between a host and its intestinal resident bacteria can transform how we understand adaptive phenotypic traits. The interplay between hosts and their resident bacteria inevitably affects the intestinal environment and, thereby, the living conditions of both the host and the microbiota. Thereby this co-existence likely influences the fitness of both bacteria and host. Whether this co-existence leads to evolutionary co-diversification in animals is largely unexplored, mainly due to the complexity of the environment and microbial communities and the often low host selection. We present the gut metagenome from wild Atlantic salmon (Salmo salar), a new wild organism model with an intestinal microbiota of low complexity and a well-described population structure, making it well-suited for investigating co-evolution. Our data reveal a strong host selection of a core gut microbiota dominated by a single Mycoplasma species. We found a clear co-diversification between the population structure of Atlantic salmon and nucleotide variability of the intestinal Mycoplasma populations conforming to expectations from co-evolution between host and resident bacteria. Our results show that the stable microbiota of Atlantic salmon has evolved with its salmonid host populations while potentially providing adaptive traits to the salmon host populations, including defence mechanisms, biosynthesis of essential amino acids, and metabolism of B vitamins. We highlight Atlantic salmon as a novel model for studying co-evolution between vertebrate hosts and their resident bacteria.

A strategic model of a host-microbe-microbe system reveals the importance of a joint host-microbe immune response to combat stress-induced gut dysbiosis.

Microbiomes provide key ecological functions to their host; however, most host-associated microbiomes are too complicated to allow a model of essential host-microbe-microbe interactions. The intestinal microbiota of salmonids may offer a solution since few dominating species often characterize it. Healthy fish coexist with a mutualistic Mycoplasma sp. species, while stress allows the spread of pathogenic strains, such as Aliivibrio sp. Even after a skin infection, the Mycoplasma does not recover; Aliivibrio sp. often remains the dominant species, or Mycoplasma-Aliivibrio coexistence was occasionally observed. We devised a model involving interactions among the host immune system, Mycoplasma sp. plus a toxin-producing pathogen. Our model embraces a complete microbiota community and is in harmony with experimental results that host-Mycoplasma mutualism prevents the spread of pathogens. Contrary, stress suppresses the host immune system allowing dominance of pathogens, and Mycoplasma does not recover after stress disappears.

Microbiome "Inception": an Intestinal Cestode Shapes a Hierarchy of Microbial Communities Nested within the Host.

The concept of a holobiont, a host organism and its associated microbial communities, encapsulates the vital role the microbiome plays in the normal functioning of its host. Parasitic infections can disrupt this relationship, leading to dysbiosis. However, it is increasingly recognized that multicellular parasites are themselves holobionts. Intestinal parasites share space with the host gut microbiome, creating a system of nested microbiomes within the primary host. However, how the parasite, as a holobiont, interacts with the host holobiont remains unclear, as do the consequences of these interactions for host health. Here, we used 16S amplicon and shotgun metagenomics sequencing to characterize the microbiome of the intestinal cestode Eubothrium and its effect on the gut microbiome of its primary host, Atlantic salmon. Our results indicate that cestode infection is associated with salmon gut dysbiosis by acting as a selective force benefiting putative pathogens and potentially introducing novel bacterial species to the host. Our results suggest that parasitic cestodes may themselves be holobionts nested within the microbial community of their holobiont host, emphasizing the importance of also considering microbes associated with parasites when studying intestinal parasitic infections. IMPORTANCE The importance of the parasite microbiome is gaining recognition. Of particular concern is understanding how these parasite microbiomes influence host-parasite interactions and parasite interactions with the vertebrate host microbiome as part of a system of nested holobionts. However, there are still relatively few studies focusing on the microbiome of parasitic helminths in general and almost none on cestodes in particular, despite the significant burden of disease caused by these parasites globally. Our study provides insights into a system of significance to the aquaculture industry, cestode infections of Atlantic salmon and, more broadly, expands our general understanding of parasite-microbiome-host interactions and introduces a new element, the microbiome of the parasite itself, which may play a critical role in modulating the host microbiome, and, therefore, the host response, to parasite infection.

Genome-resolved metagenomics suggests a mutualistic relationship between Mycoplasma and salmonid hosts.

Salmonids are important sources of protein for a large proportion of the human population. Mycoplasma species are a major constituent of the gut microbiota of salmonids, often representing the majority of microbiota. Despite the frequent reported dominance of salmonid-related Mycoplasma species, little is known about the phylogenomic placement, functions and potential evolutionary relationships with their salmonid hosts. In this study, we utilise 2.9 billion metagenomic reads generated from 12 samples from three different salmonid host species to I) characterise and curate the first metagenome-assembled genomes (MAGs) of Mycoplasma dominating the intestines of three different salmonid species, II) establish the phylogeny of these salmonid candidate Mycoplasma species, III) perform a comprehensive pangenomic analysis of Mycoplasma, IV) decipher the putative functionalities of the salmonid MAGs and reveal specific functions expected to benefit the host. Our data provide a basis for future studies examining the composition and function of the salmonid microbiota.

Salmon gut microbiota correlates with disease infection status: potential for monitoring health in farmed animals.

BACKGROUND: Infectious diseases cause significant production losses in aquaculture every year. Since the gut microbiota plays an essential role in regulating the host immune system, health and physiology, altered gut microbiota compositions are often associated with a diseased status. However, few studies have examined the association between disease severity and degree of gut dysbiosis, especially when the gut is not the site of the primary infection. Moreover, there is a lack of knowledge on whether bath treatment with formalin, a disinfectant commonly used in aquaculture to treat external infections, might affect the gut microbiome as a consequence of formalin ingestion. Here we investigate, through 16S rRNA gene metabarcoding, changes in the distal gut microbiota composition of a captive-reared cohort of 80 Atlantic salmon (Salmo salar L.), in consequence of an external bacterial skin infection due to a natural outbreak and subsequent formalin treatment. RESULTS: We identified Tenacibaculum dicentrarchi as the causative disease pathogen and we show that the distal gut of diseased salmon presented a different composition from that of healthy individuals. A new, yet undescribed, Mycoplasma genus characterized the gut of healthy salmon, while in the sick fish we observed an increase in terms of relative abundance of Aliivibrio sp., a strain regarded as opportunistic. We also noticed a positive correlation between fish weight and Mycoplasma sp. relative abundance, potentially indicating a beneficial effect for its host. Moreover, we observed that the gut microbiota of fish treated with formalin was more similar to those of sick fish than healthy ones. CONCLUSIONS: We conclude that external Tenacibaculum infections have the potential of indirectly affecting the host gut microbiota. As such, treatment optimization procedures should account for that. Formalin treatment is not an optimal solution from a holistic perspective, since we observe an altered gut microbiota in the treated fish. We suggest its coupling with a probiotic treatment aimed at re-establishing a healthy community. Lastly, we have observed a positive correlation of Mycoplasma sp. with salmon health and weight, therefore we encourage further investigations towards its potential utilization as a biomarker for monitoring health in salmon and potentially other farmed fish species.

Molecular parallelisms between pigmentation in the avian iris and the integument of ectothermic vertebrates.

Birds exhibit striking variation in eye color that arises from interactions between specialized pigment cells named chromatophores. The types of chromatophores present in the avian iris are lacking from the integument of birds or mammals, but are remarkably similar to those found in the skin of ectothermic vertebrates. To investigate molecular mechanisms associated with eye coloration in birds, we took advantage of a Mendelian mutation found in domestic pigeons that alters the deposition of yellow pterin pigments in the iris. Using a combination of genome-wide association analysis and linkage information in pedigrees, we mapped variation in eye coloration in pigeons to a small genomic region of ~8.5kb. This interval contained a single gene, SLC2A11B, which has been previously implicated in skin pigmentation and chromatophore differentiation in fish. Loss of yellow pigmentation is likely caused by a point mutation that introduces a premature STOP codon and leads to lower expression of SLC2A11B through nonsense-mediated mRNA decay. There were no substantial changes in overall gene expression profiles between both iris types as well as in genes directly associated with pterin metabolism and/or chromatophore differentiation. Our findings demonstrate that SLC2A11B is required for the expression of pterin-based pigmentation in the avian iris. They further highlight common molecular mechanisms underlying the production of coloration in the iris of birds and skin of ectothermic vertebrates.

Metagenomic analysis of historical herbarium specimens reveals a postmortem microbial community.

Advances in DNA extraction and next-generation sequencing have made a vast number of historical herbarium specimens available for genomic investigation. These specimens contain not only genomic information from the individual plants themselves, but also from associated microorganisms such as bacteria and fungi. These microorganisms may have colonized the living plant (e.g., pathogens or host-associated commensal taxa) or may result from postmortem colonization that may include decomposition processes or contamination during sample handling. Here we characterize the metagenomic profile from shotgun sequencing data from herbarium specimens of two widespread plant species (Ambrosia artemisiifolia and Arabidopsis thaliana) collected up to 180 years ago. We used blast searching in combination with megan and were able to infer the metagenomic community even from the oldest herbarium sample. Through comparison with contemporary plant collections, we identify three microbial species that are nearly exclusive to herbarium specimens, including the fungus Alternaria alternata, which can comprise up to 7% of the total sequencing reads. This species probably colonizes the herbarium specimens during preparation for mounting or during storage. By removing the probable contaminating taxa, we observe a temporal shift in the metagenomic composition of the invasive weed Am. artemisiifolia. Our findings demonstrate that it is generally possible to use herbarium specimens for metagenomic analyses, but that the results should be treated with caution, as some of the identified species may be herbarium contaminants rather than representing the natural metagenomic community of the host plant.