Exposure to crop production alters cecal prokaryotic microbiota, inflates virulome and resistome in wild prairie grouse.

Chemically intensive crop production depletes wildlife food resources, hinders animal development, health, survival, and reproduction, and it suppresses wildlife immune systems, facilitating emergence of infectious diseases with excessive mortality rates. Gut microbiota is crucial for wildlife's response to environmental stressors. Its composition and functionality are sensitive to diet changes and environmental pollution associated with modern crop production. In this study we use shotgun metagenomics (median 8,326,092 sequences/sample) to demonstrate that exposure to modern crop production detrimentally affects cecal microbiota of sharp-tailed grouse (Tympanuchus phasianellus: 9 exposed, 18 unexposed and greater prairie chickens (T. cupido; 11, 11). Exposure to crop production had greater effect on microbiota richness (t = 6.675, P < 0.001) and composition (PERMANOVA r2 = 0.212, P = 0.001) than did the host species (t = 4.762, P < 0.001; r2 = 0.070, P = 0.001) or their interaction (t = 3.449; r2 = 0.072, both P = 0.001), whereas sex and age had no effect. Although microbiota richness was greater in exposed (T. cupido chao1 = 152.8 ± 20.5; T. phasianellus 115.3 ± 17.1) than in unexposed (102.9 ± 15.1 and 101.1 ± 17.2, respectively) birds, some beneficial bacteria dropped out of exposed birds' microbiota or declined and were replaced by potential pathogens. Exposed birds also had higher richness and load of virulome (mean ± standard deviation; T. cupido 24.8 ± 10.0 and 10.1 ± 5.5, respectively; T. phasianellus 13.4 ± 6.8/4.9 ± 2.8) and resistome (T. cupido 46.8 ± 11.7/28.9 ± 10.2, T. phasianellus 38.3 ± 16.7/18.9 ± 14.2) than unexposed birds (T. cupido virulome: 14.2 ± 13.5, 4.5 ± 4.2; T. cupido resistome: 31.6 ± 20.2 and 13.1 ± 12.0; T. phasianellus virulome: 5.2 ± 4.7 and 1.4 ± 1.5; T. phasianellus resistome: 13.7 ± 16.1 and 4.0 ± 6.4).

Mangrove diversity is more than fringe deep.

Mangroves form coastal tropical forests in the intertidal zone and are an important component of shoreline protection. In comparison to other tropical forests, mangrove stands are thought to have relatively low genetic diversity with population genetic structure gradually increasing with distance along a coastline. We conducted genetic analyses of mangrove forests across a range of spatial scales; within a 400 m2 parcel comprising 181 Rhizophora mangle (red mangrove) trees, and across four sites ranging from 6-115 km apart in Honduras. In total, we successfully genotyped 269 R. mangle trees, using a panel of 677 SNPs developed with 2b-RAD methodology. Within the 400 m2 parcel, we found two distinct clusters with high levels of genetic differentiation (FST = 0.355), corresponding to trees primarily located on the seaward fringe and trees growing deeper into the forest. In contrast, there was limited genetic differentiation (FST = 0.027-0.105) across the sites at a larger scale, which had been predominantly sampled along the seaward fringe. Within the 400 m2 parcel, the cluster closest to the seaward fringe exhibited low genetic differentiation (FST = 0.014-0.043) with the other Honduran sites, but the cluster further into the forest was highly differentiated from them (FST = 0.326-0.414). These findings contradict the perception that genetic structure within mangroves forests occurs mainly along a coastline and highlights that there is greater genetic structure at fine spatial scales.

Effects of low pH on the coral reef cryptic invertebrate communities near CO2 vents in Papua New Guinea.

Small cryptic invertebrates (the cryptofauna) are extremely abundant, ecologically important, and species rich on coral reefs. Ongoing ocean acidification is likely to have both direct effects on the biology of these organisms, as well as indirect effects through cascading impacts on their habitats and trophic relationships. Naturally acidified habitats have been important model systems for studying these complex interactions because entire communities that are adapted to these environmental conditions can be analyzed. However, few studies have examined the cryptofauna because they are difficult to census quantitatively in topographically complex habitats and are challenging to identify. We addressed these challenges by using Autonomous Reef Monitoring Structures (ARMS) for sampling reef-dwelling invertebrates >2 mm in size and by using DNA barcoding for taxonomic identifications. The study took place in Papua New Guinea at two reef localities, each with three sites at varying distances from carbon dioxide seeps, thereby sampling across a natural gradient in acidification. We observed sharp overall declines in both the abundance (34-56%) and diversity (42-45%) of organisms in ARMS under the lowest pH conditions sampled (7.64-7.75). However, the overall abundance of gastropods increased slightly in lower pH conditions, and crustacean and gastropod families exhibited varying patterns. There was also variability in response between the two localities, despite their close proximity, as one control pH site displayed unusually low diversity and abundances for all invertebrate groups. The data illustrate the complexity of responses of the reef fauna to pH conditions, and the role of additional factors that influence the diversity and abundance of cryptic reef invertebrates.

Microbial symbionts and ecological divergence of Caribbean sponges: A new perspective on an ancient association.

Marine sponges host diverse communities of microbial symbionts that expand the metabolic capabilities of their host, but the abundance and structure of these communities is highly variable across sponge species. Specificity in these interactions may fuel host niche partitioning on crowded coral reefs by allowing individual sponge species to exploit unique sources of carbon and nitrogen, but this hypothesis is yet to be tested. Given the presence of high sponge biomass and the coexistence of diverse sponge species, the Caribbean Sea provides a unique system in which to investigate this hypothesis. To test for ecological divergence among sympatric Caribbean sponges and investigate whether these trends are mediated by microbial symbionts, we measured stable isotope (δ13C and δ15N) ratios and characterized the microbial community structure of sponge species at sites within four regions spanning a 1700 km latitudinal gradient. There was a low (median of 8.2 %) overlap in the isotopic niches of sympatric species; in addition, host identity accounted for over 75% of the dissimilarity in both δ13C and δ15N values and microbiome community structure among individual samples within a site. There was also a strong phylogenetic signal in both δ15N values and microbial community diversity across host phylogeny, as well as a correlation between microbial community structure and variation in δ13C and δ15N values across samples. Together, this evidence supports a hypothesis of strong evolutionary selection for ecological divergence across sponge lineages and suggests that this divergence is at least partially mediated by associations with microbial symbionts.

Does solar irradiation drive community assembly of vulture plumage microbiotas?

BACKGROUND: Stereotyped sunning behaviour in birds has been hypothesized to inhibit keratin-degrading bacteria but there is little evidence that solar irradiation affects community assembly and abundance of plumage microbiota. The monophyletic New World vultures (Cathartiformes) are renowned for scavenging vertebrate carrion, spread-wing sunning at roosts, and thermal soaring. Few avian species experience greater exposure to solar irradiation. We used 16S rRNA sequencing to investigate the plumage microbiota of wild individuals of five sympatric species of vultures in Guyana. RESULTS: The exceptionally diverse plumage microbiotas (631 genera of Bacteria and Archaea) were numerically dominated by bacterial genera resistant to ultraviolet (UV) light, desiccation, and high ambient temperatures, and genera known for forming desiccation-resistant endospores (phylum Firmicutes, order Clostridiales). The extremophile genera Deinococcus (phylum Deinococcus-Thermus) and Hymenobacter (phylum, Bacteroidetes), rare in vertebrate gut microbiotas, accounted for 9.1% of 2.7 million sequences (CSS normalized and log2 transformed). Five bacterial genera known to exhibit strong keratinolytic capacities in vitro (Bacillus, Enterococcus, Pseudomonas, Staphylococcus, and Streptomyces) were less abundant (totaling 4%) in vulture plumage. CONCLUSIONS: Bacterial rank-abundance profiles from melanized vulture plumage have no known analog in the integumentary systems of terrestrial vertebrates. The prominence of UV-resistant extremophiles suggests that solar irradiation may play a significant role in the assembly of vulture plumage microbiotas. Our results highlight the need for controlled in vivo experiments to test the effects of UV on microbial communities of avian plumage.

Distinct microbiotas of anatomical gut regions display idiosyncratic seasonal variation in an avian folivore.

BACKGROUND: Current knowledge about seasonal variation in the gut microbiota of vertebrates is limited to a few studies based on mammalian fecal samples. Seasonal changes in the microbiotas of functionally distinct gut regions remain unexplored. We investigated seasonal variation (summer versus winter) and regionalization of the microbiotas of the crop, ventriculus, duodenum, cecum, and colon of the greater sage-grouse (Centrocercus urophasianus), an avian folivore specialized on the toxic foliage of sagebrush (Artemesia spp.) in western North America. RESULTS: We sequenced the V4 region of the 16S rRNA gene on an Illumina MiSeq and obtained 6,639,051 sequences with a median of 50,232 per sample. These sequences were assigned to 457 bacterial and 4 archaeal OTUs. Firmicutes (53.0%), Bacteroidetes (15.2%), Actinobacteria (10.7%), and Proteobacteria (10.1%)were the most abundant and diverse phyla. Microbial composition and richness showed significant differences among gut regions and between summer and winter. Gut region explained almost an order of magnitude more variance in our dataset than did season or the gut region × season interaction. The effect of season was uneven among gut regions. Microbiotas of the crop and cecum showed the greatest seasonal differences. CONCLUSIONS: Our data suggest that seasonal differences in gut microbiota reflect seasonal variation in the microbial communities associated with food and water. Strong differentiation and uneven seasonal changes in the composition and richness of the microbiota among functionally distinct gut regions demonstrate the necessity of wider anatomical sampling for studies of composition and dynamics of the gut microbiota.

Publisher Correction: Spatial Organization of the Gastrointestinal Microbiota in Urban Canada Geese.

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Spatial Organization of the Gastrointestinal Microbiota in Urban Canada Geese.

Recent reviews identified the reliance on fecal or cloacal samples as a significant limitation hindering our understanding of the avian gastrointestinal (gut) microbiota and its function. We investigated the microbiota of the esophagus, duodenum, cecum, and colon of a wild urban population of Canada goose (Branta canadensis). From a population sample of 30 individuals, we sequenced the V4 region of the 16S SSU rRNA on an Illumina MiSeq and obtained 8,628,751 sequences with a median of 76,529 per sample. These sequences were assigned to 420 bacterial OTUs and a single archaeon. Firmicutes, Proteobacteria, and Bacteroidetes accounted for 90% of all sequences. Microbiotas from the four gut regions differed significantly in their richness, composition, and variability among individuals. Microbial communities of the esophagus were the most distinctive whereas those of the colon were the least distinctive, reflecting the physical downstream mixing of regional microbiotas. The downstream mixing of regional microbiotas was also responsible for the majority of observed co-occurrence patterns among microbial families. Our results indicate that fecal and cloacal samples inadequately represent the complex patterns of richness, composition, and variability of the gut microbiota and obscure patterns of co-occurrence of microbial lineages.

Variation in species diversity and functional traits of sponge communities near human populations in Bocas del Toro, Panama.

Recent studies have renewed interest in sponge ecology by emphasizing the functional importance of sponges in a broad array of ecosystem services. Many critically important habitats occupied by sponges face chronic stressors that might lead to alterations in their diversity, relatedness, and functional attributes. We addressed whether proximity to human activity might be a significant factor in structuring sponge community composition, as well as potential functional roles, by monitoring sponge diversity and abundance at two structurally similar sites that vary in distance to areas of high coastal development in Bocas Del Toro, Panama. We surveyed sponge communities at each site using belt transects and differences between two sites were compared using the following variables: (1) sponge species richness, Shannon diversity, and inverse Simpson's diversity; (2) phylogenetic diversity; (3) taxonomic and phylogenetic beta diversity; (4) trait diversity and dissimilarity; and (5) phylogenetic and trait patterns in community structure. We observed significantly higher sponge diversity at Punta Caracol, the site most distant from human development (∼5 km). Although phylogenetic diversity was lower at Saigon Bay, the site adjacent to a large village including many houses, businesses, and an airport, the sites did not exhibit significantly different patterns of phylogenetic relatedness in species composition. However, each site had a distinct taxonomic and phylogenetic composition (beta diversity). In addition, the sponge community at Saigon included a higher relative abundance of sponges with high microbial abundance and high chlorophyll a concentration, whereas the community at Punta Caracol had a more even distribution of these traits, yielding a significant difference in functional trait diversity between sites. These results suggest that lower diversity and potentially altered community function might be associated with proximity to human populations. This study highlights the importance of evaluating functional traits and phylogenetic diversity in addition to common diversity metrics when assessing potential environmental impacts on benthic communities.

Phylogenetic novelties and geographic anomalies among tropical Verongida.

Exploring marine sponges from shallow tropical reefs of the Caribbean and western Central Pacific, as part of large biodiversity (Moorea Biocode Project) and evolutionary (Porifera Tree of Life) research projects, we encountered 13 skeleton-less specimens, initially divided in two morphological groups, which had patterns of coloration and oxidation typical of taxa of the order Verongida (Demospongiae). The first group of samples inhabited open and cryptic habitats of shallow (15-20 m) Caribbean reefs at Bocas del Toro Archipelago, Panama. The second group inhabited schiophilous (e.g., inner coral framework and crevices) habitats on shallow reefs (0.5-20 m deep) in Moorea Island, French Polynesia. We applied an integrative approach by combining analyses of external morphology, histological observations, 18S rDNA, and mtCOI to determine the identity and the relationships of these unknown taxa within the order Verongida. Molecular analyses revealed that none of the species studied belonged to Hexadella (Ianthellidae, Verongida), the only fibreless genus of the Order Verongida currently recognized. The species from the Caribbean locality of Bocas del Toro (Panama) belong to the family Ianthellidae and is closely related to the Pacific genera Ianthella and Anomoianthella, both with well-developed fiber reticulations. We suggest the erection of a new generic denomination to include this novel eurypylous, fibreless ianthellid. The species collected in Moorea were all diplodal verongid taxa, with high affinities to a clade containing Pseudoceratina, Verongula, and Aiolochroia, a Pacific and two Caribbean genera, respectively. These unknown species represented at least three different taxa distinguished by DNA sequence analysis and morphological characteristics. Two new genera and a new species of Pseudoceratina are here proposed to accommodate these novel biological discoveries. The evolutionary and ecological meaning of having or lacking a fiber skeleton within Verongida is challenged under the evidence of the existence of fibreless genera within various verongid clades. Furthermore, the discovery of a fibreless Peudoceratina suggests that the possession of a spongin-chitin fiber reticulation is an "ecological" plastic trait that might be lost under certain conditions, such us growing within another organism's skeletal framework. These results raise new questions about the ecological and evolutionary significance of the development of a fiber skeleton and of sponges' adaptability to various environmental conditions.