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Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms.

ABSTRACT: Understanding the microbial degradation of Microcystis biomass is crucial for determining the ecological consequences of Microcystis blooms in freshwater lakes. The purpose of this study was to identify bacteria involved in the anaerobic degradation of Microcystis blooms. Microcystis scum was anaerobically incubated for 90 days at three temperatures (15?°C, 25?°C and 35?°C). We used terminal restriction fragment length polymorphism (T-RFLP) analysis of bacterial 16S rRNA genes, followed by cloning and sequencing of selected samples, to reveal the community composition of bacteria and their dynamics during decomposition. Clostridium spp. were found to be the most dominant bacteria in the incubations, accounting for 72% of the sequenced clones. Eight new clusters or subclusters (designated CLOS.1-8) were identified in the Clostridium phylogenetic tree. The bacterial populations displayed distinct successions during Microcystis decomposition. Temperature had a strong effect on the dynamics of the bacterial populations. At 15?°C, the initial dominance of a 207-bp T-RF (Betaproteobacteria) was largely substituted by a 227-bp T-RF (Clostridium, new cluster CLOS.2) at 30 days. In contrast, at 25?°C and 35?°C, we observed an alternating succession of the 227-bp T-RF and a 231-bp T-RF (Clostridium, new cluster CLOS.1) that occurred more than four times; no one species dominated the flora for the entire experiment. Our study shows that novel Clostridium clusters and their diverse consortiums dominate the bacterial communities during anaerobic degradation of Microcystis, suggesting that these microbes' function in the degradation process.

SUBMITTER: Xing P

PROVIDER: S-EPMC3105768 | biostudies-literature | 2011 May

REPOSITORIES: biostudies-literature

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Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms.

Xing Peng P Guo Liang L Tian Wei W Wu Qinglong L QL

The ISME journal 20101125 5

Understanding the microbial degradation of Microcystis biomass is crucial for determining the ecological consequences of Microcystis blooms in freshwater lakes. The purpose of this study was to identify bacteria involved in the anaerobic degradation of Microcystis blooms. Microcystis scum was anaerobically incubated for 90 days at three temperatures (15 °C, 25 °C and 35 °C). We used terminal restriction fragment length polymorphism (T-RFLP) analysis of bacterial 16S rRNA genes, followed by cloni ...[more]

PMID: 21107445

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Project description:In the oligotrophic oceans, key autotrophs depend on "helper" bacteria to reduce oxidative stress from hydrogen peroxide (H2O2) in the extracellular environment. H2O2 is also a ubiquitous stressor in freshwaters, but the effects of H2O2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H2O2 in freshwater systems is proposed to impact the proportion of microcystin-producing (toxic) and non-microcystin-producing (nontoxic) Microcystis in blooms, which influences toxin concentrations and human health impacts. However, how different strains of Microcystis respond to naturally occurring H2O2 concentrations and the microbes responsible for H2O2 decomposition in freshwater cyanobacterial blooms are unknown. To address these knowledge gaps, we used metagenomics and metatranscriptomics to track the presence and expression of genes for H2O2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H2O2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H2O2 scavenger (pyruvate) significantly improved growth rates of one toxic strain while other toxic and nontoxic strains were unaffected. These results indicate that heterotrophic bacteria play a key role in H2O2 decomposition in Microcystis blooms and suggest that their activity may affect the fitness of some Microcystis strains and thus the strain composition of Microcystis blooms but not along a toxic versus nontoxic dichotomy. IMPORTANCE Cyanobacterial harmful algal blooms (CHABs) threaten freshwater ecosystems globally through the production of toxins. Toxin production by cyanobacterial species and strains during CHABs varies widely over time and space, but the ecological drivers of the succession of toxin-producing species remain unclear. Hydrogen peroxide (H2O2) is ubiquitous in natural waters, inhibits microbial growth, and may determine the relative proportions of Microcystis strains during blooms. However, the mechanisms and organismal interactions involved in H2O2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H2O2 by associated heterotrophic bacteria, which may impact bloom development.

Project description:A large proportion of prokaryotic microbes in marine sediments remains uncultured, hindering our understanding of their ecological functions and metabolic features. Recent environmental metagenomic studies suggested that many of these uncultured microbes contribute to the degradation of organic matter, accompanied by acetogenesis, but the supporting experimental evidence is limited. Estuarine sediments were incubated with different types of organic matters under anaerobic conditions, and the increase of uncultured bacterial populations was monitored. We found that (1) lignin stimulated the increase of uncultured bacteria within the class Dehalococcoidia. Their ability to metabolize lignin was further supported by the presence of genes associated with a nearly complete degradation pathway of phenolic monomers in the Dehalococcoidia metagenome-assembled genomes (MAGs). (2) The addition of cellulose stimulated the increase of bacteria in the phylum Ca. Fermentibacterota and family Fibrobacterales, a high copy number of genes encoding extracellular endoglucanase or/and 1,4-beta-cellobiosidase for cellulose decomposition and multiple sugar transporters were present in their MAGs. (3) Uncultured lineages in the order Bacteroidales and the family Leptospiraceae were enriched by the addition of casein and oleic acid, respectively, a high copy number of genes encoding extracellular peptidases, and the complete β-oxidation pathway were found in those MAGs of Bacteroidales and Leptospiraceae, respectively. (4) The growth of unclassified bacteria of the order Clostridiales was found after the addition of both casein and cellulose. Their MAGs contained multiple copies of genes for extracellular peptidases and endoglucanase. Additionally, 13C-labeled acetate was produced in the incubations when 13C-labeled dissolved inorganic carbon was provided. Our results provide new insights into the roles of microorganisms during organic carbon degradation in anaerobic estuarine sediments and suggest that these macro and single molecular organic carbons support the persistence and increase of uncultivated bacteria. Acetogenesis is an additional important microbial process alongside organic carbon degradation. Video Abstract.

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Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms.

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Novel Clostridium populations involved in the anaerobic degradation of Microcystis blooms.

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