Hilary G. Morrison

The roles of marine microbes in ecosystem processes are inherently linked to their ability to sense, respond, and ultimately adapt to environmental change. Capturing the nuances of this perpetual dialogue and its long-term implications requires insight into the subtle drivers of microbial responses to environmental change that are most accessible at the shortest scales of time. Here, we present a multi-omics dataset comprising surface ocean metagenomes, metatranscriptomes, tRNA transcripts, and biogeochemical measurements, collected every 1.5 hours for 48 hours at two stations within coastal and adjacent offshore waters of the tropical Pacific Ocean. We expect that this integrated dataset of multiple sequence types and environmental parameters will facilitate novel insights into microbial ecology, microbial physiology, and ocean biogeochemistry and help investigate the different mechanisms of adaptation that drive microbial responses to environmental change.

Subsurface environments are among Earth’s largest habitats for microbial life. Yet, until recently, we lacked adequate data to accurately differentiate between globally distributed marine and terrestrial surface and subsurface microbiomes. Here, we analyzed 478 archaeal and 964 bacterial metabarcoding datasets and 147 metagenomes from diverse and widely distributed environments. Microbial diversity is similar in marine and terrestrial microbiomes at local to global scales. However, community composition greatly differs between sea and land, corroborating a phylogenetic divide that mirrors patterns in plant and animal diversity. In contrast, community composition overlaps between surface to subsurface environments supporting a diversity continuum rather than a discrete subsurface biosphere. Differences in microbial life thus seem greater between land and sea than between surface and subsurface. Diversity of terrestrial microbiomes decreases with depth, while marine subsurface diversity and phylogenetic distance to cultured isolates rivals or exceeds that of surface environments. We identify distinct microbial community compositions but similar microbial diversity for Earth’s subsurface and surface environments.

The exchange of antibiotic production and resistance genes between microorganisms can lead to the emergence of new pathogens. In this study, short-read mapping of metagenomic samples taken over time from the illeal pouch of a patient with ulcerative colitis to a Bacteroides fragilis metagenome-assembled genome revealed two distinct genomic arrangements of a novel conjugative transposon, CTn214, that encodes tetracycline resistance. The autonomous amplification of a plasmid-like circular form from CTn214 that includes tetQ potentially provides consistent ribosome protection against tetracycline. This mode of antibiotic resistance offers a novel mechanism for understanding the emergence of pathobionts like B. fragilis and their persistence for extended periods of time in patients with inflammatory bowel disease.

Soil microbial communities are fundamental to ecosystem processes and plant growth, yet community composition is seasonally and successionally dynamic, which interferes with long-term iterative experimentation of plant–microbe interactions. We explore how soil sample handling (e.g. filtering) and sample storage conditions impact the ability to revive the original, physiologically active, soil microbial community. We obtained soil from agricultural fields in Montana and Oklahoma, USA and samples were sieved to 2 mm or filtered to 45 µm. Sieved and filtered soil samples were archived at −20°C or −80°C for 50 days and revived for 2 or 7 days. We extracted DNA and the more transient RNA pools from control and treatment samples and characterized microbial communities using 16S amplicon sequencing. Filtration and storage treatments significantly altered soil microbial communities, impacting both species richness and community composition. Storing sieved soil at −20°C did not alter species richness and resulted in the least disruption to the microbial community composition in comparison to nonarchived controls as characterized by RNA pools from soils of both sites. Filtration significantly altered composition but not species richness. Archiving sieved soil at −20°C could allow for long-term and repeated experimentation on preserved physiologically active microbial communities.

Marine and terrestrial subsurface sediments, rocks, and water may represent the largest habitat for microbial life on Earth. Despite the global importance of subsurface ecosystems for biogeochemical cycling and microbial diversity, essential questions remain unanswered. These concern the abundance of novel microbial clades in the subsurface, the difference between marine and terrestrial microbiomes, as well as between subsurface and surface microbiomes, and the adaptation of specific clades to environmental conditions of the subsurface. Here, we analyzed 523 archaeal and 1,211 bacterial 16S rRNA gene amplicon sequence datasets and 146 shotgun metagenomes from surface, interface, and subsurface ecosystems worldwide, including lakes, saltmarshes, hot springs, caves, mines, methane seeps, hydrothermal vents, and seafloor sediments. We found that archaeal and bacterial alpha diversity (per sample richness and evenness) and beta diversity (community differentiation) varied continuously between surface and subsurface biomes, but differed abruptly between marine and terrestrial subsurface ecosystems. Bacterial alpha diversity tended to be lower in subsurface than surface ecosystems. However, subsurface archaeal alpha diversity often exceeded that of surface ecosystems suggesting that the subsurface holds a considerable and largely underestimated fraction of Earth’s archaeal diversity. Overall, microbial communities of marine subsurface ecosystems exhibited greater alpha diversity, while gamma diversity (total richness and evenness) was higher in the terrestrial subsurface, potentially due to greater habitat diversity. We identify diagnostic clades, especially for the archaea, that are widespread in marine (e.g., Lokiarchaeia, Bathyarchaeia) and terrestrial (e.g., Hadarchaeia, Methanococci) subsurface ecosystems. The substantial community overlap along depth transects and between surface, interface and subsurface realms suggests a global gradient between the surface and subsurface rather than a discrete and defined subsurface biosphere. Finally, none of the included subsurface ecosystems seem to be exhaustively sampled, leaving much biodiversity and metabolic capability yet to be discovered.

Background The establishment of the gut microbiome plays a key symbiotic role in the developing immune system; however, its influence on vaccine response is yet uncertain. We prospectively investigated the composition and diversity of the early-life gut microbiome in relation to infant antibody response to two routinely administered vaccines. Methods Eighty-three infants enrolled in the New Hampshire Birth Cohort Study were included in the analysis. We collected blood samples at 12 months of age and assayed the isolated serum to quantify total IgG and measured antibody to pneumococcal capsular polysaccharide and tetanus toxoid. Stool samples were collected from infants at 6 weeks of age and sequenced using 16S rRNA, and a subset of 61 samples were sequenced using shotgun metagenomics sequencing. Results We observed differences in beta diversity for 16S 6-week stool microbiota and pneumococcal and tetanus IgG antibody responses. Metagenomics analyses identified species and metabolic pathways in 6-week stool associated with tetanus antibody response, in particular, negative associations with the relative abundance of Aeriscardovia aeriphila species and positive associations with the relative abundance of species associated with CDP-diacylglycerol biosynthesis pathways. Conclusions The early gut microbiome composition may influence an infant’s vaccine response. Impact Early intestinal microbiome acquisition plays a critical role in immune maturation and in both adaptive and innate immune response in infancy. We identified associations between early life microbiome composition and response to two routinely administered vaccines—pneumococcal capsular polysaccharide and tetanus toxoid—measured at approximately 1 year of age. Our findings highlight the potential impact of the gut microbiome on infant immune response that may open up opportunities for future interventions.

By offering extremely long contiguous characterization of individual DNA molecules, rapidly emerging long‐read sequencing strategies offer comprehensive insights into the organization of genetic information in genomes and metagenomes. However, successful long‐read sequencing experiments demand high concentrations of highly purified DNA of high molecular weight (HMW), which limits the utility of established DNA extraction kits designed for short‐read sequencing. The challenges associated with input DNA quality intensify further when working with complex environmental samples of low microbial biomass, which requires new protocols that are tailored to study metagenomes with long‐read sequencing. Here, we use human tongue scrapings to benchmark six HMW DNA extraction strategies that are based on commercially available kits, phenol–chloroform (PC) extraction and agarose encasement followed by agarase digestion. A typical end goal of HMW DNA extractions is to obtain the longest possible reads during sequencing, which is often achieved by PC extractions, as demonstrated in sequencing of cultured cells. Yet our analyses that consider overall read‐size distribution, assembly performance and the number of circularized elements found in sequencing results suggest that column‐based kits with enzyme supplementation, rather than PC methods, may be more appropriate for long‐read sequencing of metagenomes.

Background: The infant intestinal microbiome plays an important role in metabolism and immune development with impacts on lifelong health. The linkage between the taxonomic composition of the microbiome and its metabolic phenotype is undefined and complicated by redundancies in the taxon-function relationship within microbial communities. To inform a more mechanistic understanding of the relationship between the microbiome and health, we performed an integrative statistical and machine learning-based analysis of microbe taxonomic structure and metabolic function in order to characterize the taxa-function relationship in early life.Results: Stool samples collected from infants enrolled in the New Hampshire Birth Cohort Study (NHBCS) at approximately 6-weeks (n = 158) and 12-months (n = 282) of age were profiled using targeted and untargeted nuclear magnetic resonance (NMR) spectroscopy as well as DNA sequencing of the V4-V5 hypervariable region from the bacterial 16S rRNA gene. There was significant inter-omic concordance based on Procrustes analysis (6 weeks:p = 0.056; 12 months:p = 0.001), however this association was no longer significant when accounting for phylogenetic relationships using generalized UniFrac distance metric (6 weeks:p = 0.376; 12 months:p = 0.069). Sparse canonical correlation analysis showed significant correlation, as well as identifying sets of microbe/metabolites driving microbiome-metabolome relatedness. Performance of machine learning models varied across different metabolites, with support vector machines (radial basis function kernel) being the consistently top ranked model. However, predictive R²values demonstrated poor predictive performance across all models assessed (avg: − 5.06% -- 6 weeks; − 3.7% -- 12 months). Conversely, the Spearman correlation metric was higher (avg: 0.344–6 weeks; 0.265–12 months). This demonstrated that taxonomic relative abundance was not predictive of metabolite concentrations.Conclusions: Our results suggest a degree of overall association between taxonomic profiles and metabolite concentrations. However, lack of predictive capacity for stool metabolic signatures reflects, in part, the possible role of functional redundancy in defining the taxa-function relationship in early life as well as the bidirectional nature of the microbiome-metabolome association. Our results provide evidence in favor of a multi-omic approach for microbiome studies, especially those focused on health outcomes.

Thousands of microbial taxa in the soil form symbioses with host plants, and due to their contribution to plant performance, these microbes are often considered an extension of the host genome. Given microbial effects on host performance, it is important to understand factors that govern microbial community assembly. Host developmental stage could affect rhizosphere microbial diversity while, alternatively, microbial assemblages could change simply as a consequence of time and the opportunity for microbial succession. Previous studies suggest that rhizosphere microbial assemblages shift across plant developmental stages, but time since germination is confounded with developmental stage. We asked how elapsed time and potential microbial succession relative to host development affected microbial diversity in the rhizosphere using monogenic flowering-time mutants of Arabidopsis thaliana. Under our experimental design, different developmental stages were present among host genotypes after the same amount of time following germination, e.g. at 76 days following germination some host genotypes were flowering while others were fruiting or senescing. We found that elapsed time was a strong predictor of microbial diversity whereas there were few differences among developmental stages. Our results support the idea that time and, likely, microbial succession more strongly affect microbial community assembly than host developmental stage.

Latitudinal diversity gradients have provided many insights into species differentiation and community processes. In the well‐studied intertidal zone, however, little is known about latitudinal diversity in microbiomes associated with habitat‐forming hosts. We investigated microbiomes of Fucus vesiculosus because of deep understanding of this model system and its latitudinally large, cross‐Atlantic range. Given multiple effects of photoperiod, we predicted that cross‐Atlantic microbiomes of the Fucus microbiome would be similar at similar latitudes and correlate with environmental factors. We found that community structure and individual amplicon sequencing variants (ASVs) showed distinctive latitudinal distributions, but alpha diversity did not. Latitudinal differentiation was mostly driven by ASVs that were more abundant in cold temperate to subarctic (e.g., Granulosicoccus_t3260, Burkholderia/Caballeronia/Paraburkholderia_t8371) or warm temperate (Pleurocapsa_t10392) latitudes. Their latitudinal distributions correlated with different humidity, tidal heights, and air/sea temperatures, but rarely with irradiance or photoperiod. Many ASVs in potentially symbiotic genera displayed novel phylogenetic biodiversity with differential distributions among tissues and regions, including closely related ASVs with differing north‐south distributions that correlated with Fucus phylogeography. An apparent southern range contraction of F. vesiculosus in the NW Atlantic on the North Carolina coast mimics that recently observed in the NE Atlantic. We suggest cross‐Atlantic microbial structure of F. vesiculosus is related to a combination of past (glacial‐cycle) and contemporary environmental drivers.