Dataset Information

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

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.

SUBMITTER: Bhatnagar S

PROVIDER: S-EPMC8066431 | biostudies-literature |

REPOSITORIES: biostudies-literature

ACCESS DATA

Similar Datasets

Project description:A harmful algal bloom occurred in late spring 2019 across multiple, interconnected fjords and bays in northern Norway. The event was caused by the haptophyte Chrysochromulina leadbeateri and led to severe fish mortality at several salmon aquaculture facilities. This study reports on the spatial and temporal succession dynamics of the holistic marine microbiome associated with this bloom by relating all detectable 18S and 16S rRNA gene amplicon sequence variants to the relative abundance of the C. leadbeateri focal taxon. A k-medoid clustering enabled inferences on how the causative focal taxon cobloomed with diverse groups of bacteria and microeukaryotes. These coblooming patterns showed high temporal variability and were distinct between two geographically separated time series stations during the regional harmful algal bloom. The distinct blooming patterns observed with respect to each station were poorly connected to environmental conditions, suggesting that other factors, such as biological interactions, may be at least as important in shaping the dynamics of this type of harmful algal bloom. A deeper understanding of microbiome succession patterns during these rare but destructive events will help guide future efforts to forecast deviations from the natural bloom cycles of the northern Norwegian coastal marine ecosystems that are home to intensive aquaculture activities. IMPORTANCE The 2019 Chrysochromulina leadbeateri bloom in northern Norway had a major impact on the local economy and society through its devastating effect on the aquaculture industry. However, many fail to remember that C. leadbeateri is, in fact, a common member of the seasonal marine microbiome and the same spring phytoplankton blooms that support the marine ecosystem. It is challenging to draw any conclusions about exact causation behind the harmful bloom of 2019, especially since the natural bloom cycles of C. leadbeateri are not well understood. This study begins to fill major knowledge gaps that may lead to future forecasting abilities, by providing a molecular-based investigation of the destructive 2019 bloom that presents new insights into a seasonal marine microbial ecosystem during one of these sporadically reoccurring events.

Project description:Harmful algal blooms (HABs) are serious ecological disasters in coastal areas, significantly influencing biogeochemical cycles driven by bacteria. The shifts in microbial communities during HABs have been widely investigated, but the assembly mechanisms of microbial communities during HABs are poorly understood. Here, using 16S rRNA gene amplicon sequencing, we analyzed the microbial communities during an early-spring diatom bloom, in order to investigate the dynamics of microbial assembly processes. Rhodobacteraceae, Flavobacteriaceae, and Microbacteriaceae were the main bacterial families during the bloom. The 30 most abundant operational taxonomic units (OTUs) segregated into 4 clusters according to specific bloom stages, exhibiting clear successional patterns during the bloom process. The succession of microbial communities correlated with changes in the dynamics of algal species. Based on the ?-nearest taxon distance, we constructed a simulation model, which demonstrated that the assembly of microbial communities shifted from strong heterogenous selection in the early stage of the bloom to stochasticity in the middle stage and then to strong homogeneous selection in the late and after-bloom stages. These successions were driven mainly by chlorophyll a contents, which were affected mainly by Skeletonema costatum Moreover, functional prediction of microbial communities showed that microbial metabolic functions were significantly related to nitrogen metabolism. In summary, our results clearly suggested a dominant role of determinacy in microbial community assembly in HABs and will facilitate deeper understanding of the ecological processes shaping microbial communities during the algal bloom process.IMPORTANCE Harmful algal blooms (HABs) significantly influence biogeochemical cycles driven by bacteria. The shifts in microbial communities during HABs have been studied intensively, but the assembly mechanisms of microbial communities during HABs are poorly understood, with limited investigation of the balance of deterministic and stochastic processes in shaping microbial communities in HABs. In this study, the dynamics and assembly of microbial communities in an early-spring diatom bloom process were investigated. Our data both confirm previously observed general microbial successional patterns and show new detailed mechanisms for microbial assembly in HABs. These results will facilitate deeper understanding of the ecological processes shaping microbial communities in HABs. In addition, predictions of metabolic potential in this study will facilitate understanding of the influence of HABs on nitrogen metabolism in marine environments.

Project description:Interactions between microorganisms and algae during bloom events significantly impacts their physiology, alters ambient chemistry, and shapes ecosystem diversity. The potential role these interactions have in bloom development and decline are also of particular interest given the ecosystem impacts of algal blooms. We hypothesized that microbial community structure and succession is linked to specific bloom stages, and reflects complex interactions among taxa comprising the phycosphere environment. This investigation used pyrosequencing and correlation approaches to assess patterns and associations among bacteria, archaea, and microeukaryotes during a spring bloom of the dinoflagellate Alexandrium catenella. Within the bacterial community, Gammaproteobacteria and Bacteroidetes were predominant during the initial bloom stage, while Alphaproteobacteria, Cyanobacteria, and Actinobacteria were the most abundant taxa present during bloom onset and termination. In the archaea biosphere, methanogenic members were present during the early bloom period while the majority of species identified in the late bloom stage were ammonia-oxidizing archaea and Halobacteriales. Dinoflagellates were the major eukaryotic group present during most stages of the bloom, whereas a mixed assemblage comprising diatoms, green-algae, rotifera, and other microzooplankton were present during bloom termination. Temperature and salinity were key environmental factors associated with changes in bacterial and archaeal community structure, respectively, whereas inorganic nitrogen and inorganic phosphate were associated with eukaryotic variation. The relative contribution of environmental parameters measured during the bloom to variability among samples was 35.3%. Interaction analysis showed that Maxillopoda, Spirotrichea, Dinoflagellata, and Halobacteria were keystone taxa within the positive-correlation network, while Halobacteria, Dictyochophyceae, Mamiellophyceae, and Gammaproteobacteria were the main contributors to the negative-correlation network. The positive and negative relationships were the primary drivers of mutualist and competitive interactions that impacted algal bloom fate, respectively. Functional predictions showed that blooms enhance microbial carbohydrate and energy metabolism, and alter the sulfur cycle. Our results suggest that microbial community structure is strongly linked to bloom progression, although specific drivers of community interactions and responses are not well understood. The importance of considering biotic interactions (e.g., competition, symbiosis, and predation) when investigating the link between microbial ecological behavior and an algal bloom's trajectory is also highlighted.