Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom
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Author(s)
Bhatnagar, Srijak
Cowley, Elise S
Kopf, Sebastian H
Pérez Castro, Sherlynette
Kearney, Sean Michael
Dawson, Scott C
Hanselmann, Kurt
Ruff, S. E
Castro, Sherlynette Pérez
Kearney, Sean
Date Issued
January 17, 2020
Journal
Environmental Microbiome
Publisher
BioMed Central
Citation
Bhatnagar, Srijak et al. "Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom." Environmental Microbiome 15, 1 (January 2020): 3 doi 10.1186/s40793-019-0348-0 ©2020 Author(s)
Version
Final published version
Abstract
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. KEYWORDS: microbial succession; green sulfur bacteria; prosthecochloris; syntrophy; brackish coastal ecosystem; anoxygenic phototrophy; microviridae; sulfur cycling; CRISPR-Cas; resilience
MIT Department
Massachusetts Institute of Technology. Department of Biological Engineering
Massachusetts Institute of Technology. Department of Civil and Environmental Engineering
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DOI of Published Version
https://doi.org/10.1186/s40793-019-0348-0
