Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Bhatnagar, S., Cowley, E. S., Kopf, S. H., Pérez Castro, S., Kearney, S., Dawson, S. C., Hanselmann, K., & Ruff, S. E. Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom. Environmental Microbiome, 15(1),(2020): 3, doi:10.1186/s40793-019-0348-0.Background: Lagoons are common along coastlines worldwide and are important for biogeochemical element cycling, coastal biodiversity, coastal erosion protection and blue carbon sequestration. These ecosystems are frequently disturbed by weather, tides, and human activities. Here, we investigated a shallow lagoon in New England. The brackish ecosystem releases hydrogen sulfide particularly upon physical disturbance, causing blooms of anoxygenic sulfur-oxidizing phototrophs. To study the habitat, microbial community structure, assembly and function we carried out in situ experiments investigating the bloom dynamics over time. Results: Phototrophic microbial mats and permanently or seasonally stratified water columns commonly contain multiple phototrophic lineages that coexist based on their light, oxygen and nutrient preferences. We describe similar coexistence patterns and ecological niches in estuarine planktonic blooms of phototrophs. The water column showed steep gradients of oxygen, pH, sulfate, sulfide, and salinity. The upper part of the bloom was dominated by aerobic phototrophic Cyanobacteria, the middle and lower parts by anoxygenic purple sulfur bacteria (Chromatiales) and green sulfur bacteria (Chlorobiales), respectively. We show stable coexistence of phototrophic lineages from five bacterial phyla and present metagenome-assembled genomes (MAGs) of two uncultured Chlorobaculum and Prosthecochloris species. In addition to genes involved in sulfur oxidation and photopigment biosynthesis the MAGs contained complete operons encoding for terminal oxidases. The metagenomes also contained numerous contigs affiliating with Microviridae viruses, potentially affecting Chlorobi. Our data suggest a short sulfur cycle within the bloom in which elemental sulfur produced by sulfide-oxidizing phototrophs is most likely reduced back to sulfide by Desulfuromonas sp. Conclusions: The release of sulfide creates a habitat selecting for anoxygenic sulfur-oxidizing phototrophs, which in turn create a niche for sulfur reducers. Strong syntrophism between these guilds apparently drives a short sulfur cycle that may explain the rapid development of the bloom. The fast growth and high biomass yield of Chlorobi-affiliated organisms implies that the studied lineages of green sulfur bacteria can thrive in hypoxic habitats. This oxygen tolerance is corroborated by oxidases found in MAGs of uncultured Chlorobi. The findings improve our understanding of the ecology and ecophysiology of anoxygenic phototrophs and their impact on the coupled biogeochemical cycles of sulfur and carbon.This work was carried out at the Microbial Diversity summer course at the Marine Biological Laboratory in Woods Hole, MA. The course was supported by grants from National Aeronautics and Space Administration, the US Department of Energy, the Simons Foundation, the Beckman Foundation, and the Agouron Institute. Additional funding for SER was provided by the Marine Biological Laboratory

Fecal Microbial Communities in a Large Representative Cohort of California Dairy Cows

Improved sequencing and analytical techniques allow for better resolution of microbial communities; however, the agriculture field lacks an updated analysis surveying the fecal microbial populations of dairy cattle in California. This study is a large-scale survey to determine the composition of the bacterial community present in the feces of lactating dairy cattle on commercial dairy operations. For the study, 10 dairy farms across northern and central California representing a variety of feeding and management systems were enrolled. The farms represented three typical housing types including five freestall, two drylot and three pasture-based management systems. Fresh feces were collected from 15 randomly selected cows on each farm and analyzed using 16S rRNA gene amplicon sequencing. This study found that housing type, individual farm, and dietary components significantly affected the alpha diversity of the fecal microbiota. While only one Operational Taxonomic Unit (OTU) was common among all the sampled individuals, 15 bacterial families and 27 genera were shared among 95% of samples. The ratio of the families Coriobacteriaceae to Bifidobacteriaceae was significantly different between housing types and farms with pasture fed animals having a higher relative abundance of Coriobacteriaceae. A majority of samples were positive for at least one OTU assigned to Enterobacteriaceae and 31% of samples contained OTUs assigned to Campylobacter. However, the relative abundance of both taxa was <0.1%. The microbial composition displays individual farm specific signatures, but housing type plays a role. These data provide insights into the composition of the core fecal microbiota of commercial dairy cows in California and will further generate hypotheses for strategies to manipulate the microbiome of cattle

Complete Genome Sequence of Curtobacterium sp. Strain MR_MD2014, Isolated from Topsoil in Woods Hole, Massachusetts

Here, we present the 3,443,800-bp complete genome sequence of Curtobacterium sp. strain MR_MD2014 (phylum Actinobacteria). This strain was isolated from soil in Woods Hole, MA, as part of the 2014 Microbial Diversity Summer Program at the Marine Biological Laboratory in Woods Hole, MA

Complete Genome Sequence of Streptomyces sp. Strain CCM_MD2014, Isolated from Topsoil in Woods Hole, Massachusetts

Here, we present the complete genome sequence of Streptomyces sp. strain CCM_MD2014 (phylum Actinobacteria), isolated from surface soil in Woods Hole, MA. Its single linear chromosome of 8,274,043 bp in length has a 72.13% G+C content and contains 6,948 coding sequences

Bacterial Communities of Diverse Drosophila Species: Ecological Context of a Host–Microbe Model System

Drosophila melanogaster is emerging as an important model of non-pathogenic host–microbe interactions. The genetic and experimental tractability of Drosophila has led to significant gains in our understanding of animal–microbial symbiosis. However, the full implications of these results cannot be appreciated without the knowledge of the microbial communities associated with natural Drosophila populations. In particular, it is not clear whether laboratory cultures can serve as an accurate model of host–microbe interactions that occur in the wild, or those that have occurred over evolutionary time. To fill this gap, we characterized natural bacterial communities associated with 14 species of Drosophila and related genera collected from distant geographic locations. To represent the ecological diversity of Drosophilids, examined species included fruit-, flower-, mushroom-, and cactus-feeders. In parallel, wild host populations were compared to laboratory strains, and controlled experiments were performed to assess the importance of host species and diet in shaping bacterial microbiome composition. We find that Drosophilid flies have taxonomically restricted bacterial communities, with 85% of the natural bacterial microbiome composed of only four bacterial families. The dominant bacterial taxa are widespread and found in many different host species despite the taxonomic, ecological, and geographic diversity of their hosts. Both natural surveys and laboratory experiments indicate that host diet plays a major role in shaping the Drosophila bacterial microbiome. Despite this, the internal bacterial microbiome represents only a highly reduced subset of the external bacterial communities, suggesting that the host exercises some level of control over the bacteria that inhabit its digestive tract. Finally, we show that laboratory strains provide only a limited model of natural host–microbe interactions. Bacterial taxa used in experimental studies are rare or absent in wild Drosophila populations, while the most abundant associates of natural Drosophila populations are rare in the lab

Identification of Factors That Drive Taxonomic, Phylogenetic, and Functional Composition of Microbial Communities Using DNA Sequence Analyses

Microbial life represents the majority of the diversity of life on planet earth. Microbes are found in all ecosystems. The microbial community of an ecosystem can be an indicator of its health and the foundation of the ecosystem function. Thus, an understanding of the microbial community of an ecosystem is vital to understanding the ecosystem itself. To fully grasp the microbial community structure, it is essential to understand the factors that shape the community composition and diversity of the ecosystem. This works focusses on the primary drivers of microbial composition in three ecosystems: an estuary, the gut of Drosophila melanogaster, and walnut grove soil. In the benthic estuarine environment of Trunk River, physical perturbations in the water column above decaying seagrass altered the composition of the microbial community causing a visible microbial bloom. To understand the microbial community progression in the bloom, we simulated perturbed sites in the river and studied four different depths in the water column for two weeks. We found the bloom was largely made up of Prosthecochloris vibrioformis, a phototrophic sulfur oxidizer. The bloom appears to be driven by pH, salinity, and sulfide gradients, forming at a depth of ≈ 25cm beneath the surface of the water. For the third chapter, we explored the effect of host diet on its gut microbial community. We created a controlled experiment in Drosophila melanogaster, a model organism. A population of D. melanogaster preconditioned on a balanced lab diet was split into two treatment diets, a high-sugar diet and a high-yeast diet. The microbial communities in the fecal matter of the flies were sampled for 4 days to understand their compositional changes. We found that a shift in the diet of D. melanogaster changed the phylogenetic, taxonomic, and functional compositions of the microbial communities. Each dietary change led to a distinct taxonomic, phylogenetic, and functional composition by the end of the experiment. The functional diversity of both treatment groups decreased, indicating a shift away from a diverse set of metabolic capabilities when subjected to a more comprehensive nutrition to a more specific set of metabolic capabilities adapted for the main nutrient, either sucrose or yeast extract. In the fourth chapter, Pesticide-treated orchard soils were used to understand the effects of deliberate intervention (external factors) on microbial ecosystems. We also studied the potential of pathogens to colonize soil that had been exposed to such external factors. In a controlled experiment, soil was subjected to different fumigation treatments with and without subsequent amendment. It was then inoculated and incubated with Agrobacterium tumefaciens. The results indicate a fumigant-specific shift in the phylogenetic, taxonomic, genic, and functional composition of the soil. The low diversity fumigated soil was also better colonized by the A. tumefaciens. However, post-fumigation amendment with vermicompost increased the diversity, shifting the compositions towards non-fumigated vermicompost and suppressing A. tumefaciens colonization. With this work, we have been able to implicate some of the important factors at play in the determination of microbial composition in various ecosystems. Additionally, we showed that the influence of these factors on microbial community is measurable on different metrics of composition