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

Bhatnagar, Srijak; Cowley, Elise S.; Kopf, Sebastian H.; Pérez Castro, Sherlynette; Kearney, Sean; Dawson, Scott C.; Hanselmann, Kurt; Ruff, S. Emil

doi:10.1186/s40793-019-0348-0

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

Journal Article · Thu Jan 16 23:00:00 EST 2020 · Environmental Microbiome

DOI:https://doi.org/10.1186/s40793-019-0348-0· OSTI ID:1816619

Bhatnagar, Srijak ^[1]; Cowley, Elise S. ^[2]; Kopf, Sebastian H. ^[3]; Pérez Castro, Sherlynette ^[4]; Kearney, Sean ^[5]; Dawson, Scott C. ^[6]; Hanselmann, Kurt ^[7]; ^[4]

Univ. of Calgary, AB (Canada)
Univ. of Wisconsin, Madison, WI (United States)
Univ. of Colorado, Boulder, CO (United States)
Marine Biological Laboratory, Woods Hole, MA (United States)
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States)
Univ. of California, Davis, CA (United States)
Eidgenoessische Technische Hochschule (ETH), Zurich (Switzerland)

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.

View Accepted Manuscript (DOE)

Research Organization:: Marine Biological Laboratory, Woods Hole, MA (United States)

Sponsoring Organization:: USDOE

OSTI ID:: 1816619

Journal Information:: Environmental Microbiome, Journal Name: Environmental Microbiome Journal Issue: 1 Vol. 15; ISSN 2524-6372

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
CRISPR-Cas
anoxygenic phototrophy
brackish coastal ecosystem
green sulfur bacteria
microbial succession
microviridae
prosthecochloris
resilience
sulfur cycling
syntrophy

Microbial diversity and physicochemistry of an estuarine phototrophic bloom in the Trunk River, Wood Hole (MA) Bhatnagar, Srijak; Cowley, Elise S.; Kopf, Sebastian https://doi.org/10.1594/pangaea.900343 The current record is supplemented by this dataset	dataset	January 2019
MOESM1 of Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom Bhatnagar, Srijak; Cowley, Elise; Kopf, Sebastian https://doi.org/10.6084/m9.figshare.11643786.v1 The current record is supplemented by this text	text	January 2020
Microbial community dynamics and coexistence in a sulfide-driven phototrophic bloom Bhatnagar, Srijak; Cowley, Elise; Kopf, Sebastian https://doi.org/10.6084/m9.figshare.c.4822512 The current record is supplemented by this collection	collection	January 2020

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

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