Minnesota peat viromes reveal terrestrial and aquatic niche partitioning for local and global viral populations

Background Peatlands are expected to experience sustained yet fluctuating higher temperatures due to climate change, leading to increased microbial activity and greenhouse gas emissions. Despite mounting evidence for viral contributions to these processes in peatlands underlain with permafrost, little is known about viruses in other peatlands. More generally, soil viral biogeography and its potential drivers are poorly understood at both local and global scales. Here, 87 metagenomes and five viral size-fraction metagenomes (viromes) from a boreal peatland in northern Minnesota (the SPRUCE whole-ecosystem warming experiment and surrounding bog) were analyzed for dsDNA viral community ecological patterns, and the recovered viral populations (vOTUs) were compared with our curated PIGEON database of 266,125 vOTUs from diverse ecosystems. Results Within the SPRUCE experiment, viral community composition was significantly correlated with peat depth, water content, and carbon chemistry, including CH4 and CO2 concentrations, but not with temperature during the first 2 years of warming treatments. Peat vOTUs with aquatic-like signatures (shared predicted protein content with marine and/or freshwater vOTUs) were significantly enriched in more waterlogged surface peat depths. Predicted host ranges for SPRUCE vOTUs were relatively narrow, generally within a single bacterial genus. Of the 4326 SPRUCE vOTUs, 164 were previously detected in other soils, mostly peatlands. None of the previously identified 202,371 marine and freshwater vOTUs in our PIGEON database were detected in SPRUCE peat, but 0.4% of 80,714 viral clusters (VCs, grouped by predicted protein content) were shared between soil and aquatic environments. On a per-sample basis, vOTU recovery was 32 times higher from viromes compared with total metagenomes. Conclusions Results suggest strong viral “species” boundaries between terrestrial and aquatic ecosystems and to some extent between peat and other soils, with differences less pronounced at higher taxonomic levels. The significant enrichment of aquatic-like vOTUs in more waterlogged peat suggests that viruses may also exhibit niche partitioning on more local scales. These patterns are presumably driven in part by host ecology, consistent with the predicted narrow host ranges. Although more samples and increased sequencing depth improved vOTU recovery from total metagenomes, the substantially higher per-sample vOTU recovery after viral particle enrichment highlights the utility of soil viromics.

Culturing Putatively Obligate Epizoic Diatoms: Insights for the Evolution and Ecology of Diatoms and Their Host

Background: Our understanding of the importance of microbiomes on large aquatic animals—such as whales, sea turtles and manatees—has advanced considerably in recent years. Recent activity describing the epizoic diatoms growing on marine vertebrates suggests that these epibiotic diatom communities constitute diverse, polyphyletic, and compositionally stable assemblages that include both putatively obligate epizoic and generalist species. Here, we outline a successful attempt to culture putatively obligate epizoic diatoms without their hosts and propose further applications and research avenues in this growing area of study. Results: We cultured cells of epizoic diatoms from multiple host species sampled in the wild and captivity. Analyzing the DNA sequences of these cultures, we found that several unique diatom taxa have independently evolved to occupy in epibiotic habitats. We created a library of reference sequence data for use in metabarcoding surveys of sea turtle and manatee microbiomes that will further facilitate the use of environmental DNA for studying host specificity in epizoic diatoms and the utility of diatoms as indicators of host ecology and health. Conclusions: Our discovery that epizoic diatoms can be cultured independently from their hosts raises several questions about the nature of the interaction between these diatom species and their hosts. We encourage the interdisciplinary community working with marine megafauna to consider including diatom sampling and diatom analysis into their routine practices.

Ormyrus labotus Walker (Hymenoptera: Ormyridae): another generalist that should not be a generalist is not a generalist

Several recent reappraisals of supposed generalist parasite species have revealed hidden complexes of species, each with considerably narrower host ranges. Parasitic wasps that attack gall-forming insects on plants have life history strategies that are thought to promote specialization, and though many species are indeed highly specialized, others have been described as generalist parasites. Ormyrus labotus Walker (Hymenoptera: Ormyridae) is one such apparent generalist, with rearing records spanning more than 65 host galls associated with a diverse set of oak tree species and plant tissues. We pair a molecular approach with morphology, host ecology, and phenological data from across a wide geographic sample to test the hypothesis that this supposed generalist is actually a complex of several more specialized species, though we identify no single unifying axis of specialization. We find 16-18 putative species within the morphological species O. labotus, each reared from only 1-6 host gall types. We also find cryptic habitat specialists within two other named Ormyrus species. Our study suggests that caution should be applied when considering host ranges of parasitic insects described solely by morphological traits, particularly given their importance as biocontrol organisms and their role in biodiversity and evolutionary studies.

Defining gut mycobiota for wild animals: a need for caution in assigning authentic resident fungal taxa

Animal gut mycobiota, the community of fungi that reside within the gastrointestinal tract, make an important contribution to host health. Accordingly, there is an emerging interest to quantify the gut mycobiota of wild animals. However, many studies of wild animal gut mycobiota do not distinguish between the fungi that likely can reside within animal gastrointestinal tracts from the fungal taxa that are non-residents, such as macrofungi, lichens or plant symbionts/pathogens that can be ingested as part of the host’s diet. Confounding the non-resident and resident gut fungi may obscure attempts to identify processes associated with the authentic, resident gut mycobiota per se. To redress this problem, we propose some strategies to filter the taxa identified within an apparent gut mycobiota based on an assessment of host ecology and fungal traits. Consideration of the different sources and roles of fungi present within the gastrointestinal tract should facilitate a more precise understanding of the causes and consequences of variation in wild animal gut mycobiota composition.

Bioclimatic and anthropogenic variables shape the occurrence of Batrachochytrium dendrobatidis over a large latitudinal gradient

Amphibian chytridiomycosis, caused by the fungus Batrachochytrium dendrobatidis (Bd), has caused the greatest known loss of biodiversity due to an infectious disease. We used Bd infection data from quantitative real-time PCR (qPCR) assays of amphibian skin swabs collected across Chile during 2008–2018 to model Bd occurrence with the aim to determine bioclimatic and anthropogenic variables associated with Bd infection. Also, we used Bd presence/absence records to identify geographical Bd high-risk areas and compare Bd prevalence and infection loads between amphibian families, ecoregions, and host ecology. Data comprised 4155 Bd-specific qPCR assays from 162 locations across a latitudinal gradient of 3700 km (18º to 51ºS). Results showed a significant clustering of Bd associated with urban centres and anthropogenically highly disturbed ecosystems in central-south Chile. Both Bd prevalence and Bd infection loads were higher in aquatic than terrestrial amphibian species. Our model indicated positive associations of Bd prevalence with altitude, temperature, precipitation and human-modified landscapes. Also, we found that macroscale drivers, such as land use change and climate, shape the occurrence of Bd at the landscape level. Our study provides with new evidence that can improve the effectiveness of strategies to mitigate biodiversity loss due to amphibian chytridiomycosis.

Host phylogeny and host ecology structure the mammalian gut microbiota at different taxonomic scales

The gut microbiota is critical for host function. Among mammals, host phylogenetic relatedness and diet are strong drivers of gut microbiota structure, but one factor may be more influential than the other. Here, we used 16S rRNA gene sequencing to determine the relative contributions of host phylogeny and host diet in structuring the gut microbiotas of 11 herbivore species from 5 families living sympatrically in southwest Kenya. Herbivore species were classified as grazers, browsers, or mixed-feeders and dietary data (% C4 grasses in diet) were compiled from previously published sources. We found that herbivore gut microbiotas were highly species-specific, and that host taxonomy accounted for more variation in the gut microbiota (30%) than did host dietary guild (10%) or sample month (8%). Overall, similarity in the gut microbiota increased with host phylogenetic relatedness (r = 0.74) across the 11 species of herbivores, but among 7 closely related Bovid species, dietary %C4 grass values more strongly predicted gut microbiota structure (r = 0.64). Additionally, within bovids, host dietary guild explained more of the variation in the gut microbiota (17%) than did host species (12%). Lastly, while we found that the gut microbiotas of herbivores residing in southwest Kenya converge with those of distinct populations of conspecifics from central Kenya, fine-scale differences in the abundances of bacterial amplicon sequence variants (ASVs) between individuals from the two regions were also observed. Overall, our findings suggest that host phylogeny and taxonomy strongly structure the gut microbiota across broad host taxonomic scales, but these gut microbiotas can be further modified by host ecology (i.e., diet, geography), especially among closely related host species.

Examining prevalence and diversity of tick-borne pathogens in questing Ixodes pacificus ticks in California.

Tick-borne diseases in California include Lyme disease (caused by Borrelia burgdorferi), infections with Borrelia miyamotoi, and human granulocytic anaplasmosis (caused by Anaplasma phagocytophilum). We surveyed multiple sites and habitats (woodland, grassland, coastal chaparral) in California to describe spatial patterns of tick-borne pathogen prevalence in western black-legged ticks (Ixodes pacificus). We found that several species of Borrelia – B. burgdorferi, B. americana and B. bissettiae - were observed in habitats such as coastal chaparral that does not harbor obvious reservoir host candidates. Describing tick-borne pathogen prevalence is strongly influenced by the scale of surveillance: aggregating data from individual sites to match jurisdictional boundaries (e.g., county or state) can lower the reported infection prevalence. Considering multiple pathogen species in the same habitat allows a more cohesive interpretation of local pathogen occurrence. Importance Understanding the local host ecology and prevalence of zoonotic diseases is vital for public health. Using tick-borne diseases in California, we show that there is often a bias to our understanding and that studies tend to focus on particular habitats e.g., Lyme disease in oak woodlands. Other habitats may harbor a surprising diversity of tick-borne pathogens but have been neglected, e.g., coastal chaparral. Explaining pathogen prevalence requires descriptions of data at a local scale; otherwise, aggregating the data can misrepresent the local dynamics of tick-borne diseases.

Surveillance of densoviruses and mesomycetozoans inhabiting grossly normal tissues of three Aotearoa New Zealand asteroid species

Asteroid wasting events and mass mortality have occurred for over a century. We currently lack a fundamental understanding of the microbial ecology of asteroid disease, with disease investigations hindered by sparse information about the microorganisms associated with grossly normal specimens. We surveilled viruses and protists associated with grossly normal specimens of three asteroid species (Patiriella regularis, Stichaster australis, Coscinasterias muricata) on the North Island / Te Ika-a-Māui, Aotearoa New Zealand, using metagenomes prepared from virus and ribosome-sized material. We discovered several densovirus-like genome fragments in our RNA and DNA metagenomic libraries. Subsequent survey of their prevalence within populations by quantitative PCR (qPCR) demonstrated their occurrence in only a few (13%) specimens (n = 36). Survey of large and small subunit rRNAs in metagenomes revealed the presence of a mesomycete (most closely matching Ichthyosporea sp.). Survey of large subunit prevalence and load by qPCR revealed that it is widely detectable (80%) and present predominately in body wall tissues across all 3 species of asteroid. Our results raise interesting questions about the roles of these microbiome constituents in host ecology and pathogenesis under changing ocean conditions.