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

Degradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Castro, S. P., Borton, M. A., Regan, K., de Angelis, I. H., Wrighton, K. C., Teske, A. P., Strous, M., & Ruff, S. E. Degradation of biological macromolecules supports uncultured microbial populations in Guaymas Basin hydrothermal sediments. Isme Journal. (2021), https://doi.org/10.1038/s41396-021-01026-5.Hydrothermal sediments contain large numbers of uncultured heterotrophic microbial lineages. Here, we amended Guaymas Basin sediments with proteins, polysaccharides, nucleic acids or lipids under different redox conditions and cultivated heterotrophic thermophiles with the genomic potential for macromolecule degradation. We reconstructed 20 metagenome-assembled genomes (MAGs) of uncultured lineages affiliating with known archaeal and bacterial phyla, including endospore-forming Bacilli and candidate phylum Marinisomatota. One Marinisomatota MAG had 35 different glycoside hydrolases often in multiple copies, seven extracellular CAZymes, six polysaccharide lyases, and multiple sugar transporters. This population has the potential to degrade a broad spectrum of polysaccharides including chitin, cellulose, pectin, alginate, chondroitin, and carrageenan. We also describe thermophiles affiliating with the genera Thermosyntropha, Thermovirga, and Kosmotoga with the capability to make a living on nucleic acids, lipids, or multiple macromolecule classes, respectively. Several populations seemed to lack extracellular enzyme machinery and thus likely scavenged oligo- or monomers (e.g., MAGs affiliating with Archaeoglobus) or metabolic products like hydrogen (e.g., MAGs affiliating with Thermodesulfobacterium or Desulforudaceae). The growth of methanogens or the production of methane was not observed in any condition, indicating that the tested macromolecules are not degraded into substrates for methanogenesis in hydrothermal sediments. We provide new insights into the niches, and genomes of microorganisms that actively degrade abundant necromass macromolecules under oxic, sulfate-reducing, and fermentative thermophilic conditions. These findings improve our understanding of the carbon flow across trophic levels and indicate how primary produced biomass sustains complex and productive ecosystems.We are grateful to the captain and crew of the R/V Atlantis AT37-06 as well as the crew of the human occupied vehicle Alvin for their tireless support. Sampling at Guaymas Basin was supported by NSF (OCE-1357238)

Soil microbial responses to drought and exotic plants shift carbon metabolism.

Significant gaps in our understanding of how global change drivers interact to affect the resistance and functioning of microbial communities hinders our ability to model ecosystem responses and feedbacks to co-occurring global stressors. Here, we investigated the effects of extreme drought and exotic plants, two of the most significant threats to Mediterranean-type ecosystems, on soil microbial community composition and carbon metabolic genes within a four-year field rainfall manipulation experiment. We combined measurements of bulk microbial and soil properties with high-throughput microbial community analyses to elucidate microbial responses and microbial-mediated alterations to carbon cycling. While microbial responses to experimental droughts were weak, scant rainfall periods resulted in decreased microbial biomass and activity, and relative abundances of bacterial groups such as Proteobacteria, Verrucomicrobia, and Acidobacteria decreased concomitantly with increases in Actinobacteria, Chloroflexi, and Firmicutes abundance. Soils under exotic plants had increased temperatures, enhanced infiltration during rainfall events, and decreased water retention and labile carbon in comparison to soils under native plants. Higher peaks and more seasonally variable microbial activity were found under exotic plants and, like drought periods, the microbial community shifted towards osmotic stress life-strategies. Relationships found between microbial taxonomic groups and carbon metabolic genes support the interpretation that exotic plants change microbial carbon cycling by altering the soil microclimate and supplying easily decomposed high-quality litter. Soil microbial community responses to drought and exotic plants could potentially impact ecosystem C storage by producing a smaller, more vulnerable C pool of microbial biomass that is prone to increased pulses of heterotrophic respiration

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

BackgroundLagoons 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.ResultsPhototrophic 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.ConclusionsThe 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

Author Correction: Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom (vol 15, 3 , 2023)

ISSN:2524-637