Evaluation of different 16S rRNA gene V regions for exploring bacterial diversity in a eutrophic freshwater lake.

Cyanobacterial blooms are a global ecological problem that directly threatens human health and crop safety. Cyanobacteria have toxic effects on aquatic microorganisms, which could drive the selection for resistance genes. The effect of cyanobacterial blooms on the dispersal and abundance of antibiotic-resistance genes (ARGs) of concern to human health remains poorly known. We herein investigated the effect of cyanobacterial blooms on ARG composition in Lake Taihu, China. The numbers and relative abundances of total ARGs increased obviously during a Planktothrix bloom. More pathogenic microorganisms were present during this bloom than during a Planktothrix bloom or during the non-bloom period. Microcosmic experiments using additional aquatic ecosystems (an urban river and Lake West) found that a coculture of Microcystis aeruginosa and Planktothrix agardhii increased the richness of the bacterial community, because its phycosphere provided a richer microniche for bacterial colonization and growth. Antibiotic-resistance bacteria were naturally in a rich position, successfully increasing the momentum for the emergence and spread of ARGs. These results demonstrate that cyanobacterial blooms are a crucial driver of ARG diffusion and enrichment in freshwater, thus providing a reference for the ecology and evolution of ARGs and ARBs and for better assessing and managing water quality.

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Cyanobacterial blooms contribute to the diversity of antibiotic-resistance genes in aquatic ecosystems

Cyanobacterial blooms are worldwide issues of societal concern and scientific interest. Lake Taihu and Lake Dianchi, two of the largest lakes in China, have been suffering from annual Microcystis-based blooms over the past two decades. These two eutrophic lakes differ in both nutrient load and environmental parameters, where Microcystis microbiota consisting of different Microcystis morphospecies and associated bacteria (epibionts) have dominated. We conducted a comprehensive metagenomic study that analyzed species diversity, community structure, functional components, metabolic pathways and networks to investigate functional interactions among the members of six Microcystis-epibiont communities in these two lakes. Our integrated metagenomic pipeline consisted of efficient assembly, binning, annotation, and quality assurance methods that ensured high-quality genome reconstruction. This study provides a total of 68 reconstructed genomes including six complete Microcystis genomes and 28 high quality bacterial genomes of epibionts belonging to 14 distinct taxa. This metagenomic dataset constitutes the largest reference genome catalog available for genome-centric studies of the Microcystis microbiome. Epibiont community composition appears to be dynamic rather than fixed, and the functional profiles of communities were related to the environment of origin. This study demonstrates mutualistic interactions between Microcystis and epibionts at genetic and metabolic levels. Metabolic pathway reconstruction provided evidence for functional complementation in nitrogen and sulfur cycles, fatty acid catabolism, vitamin synthesis, and aromatic compound degradation among community members. Thus, bacterial social interactions within Microcystis-epibiont communities not only shape species composition, but also stabilize the communities’ functional profiles. These interactions appear to play an important role in environmental adaptation of Microcystis colonies.

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A Large-Scale Comparative Metagenomic Study Reveals the Functional Interactions in Six Bloom-Forming Microcystis-Epibiont Communities.

The toxic cyanobacterium Microcystis is one of the most pervasive harmful algal bloom (HAB) genera and naturally occurs in large colonies known to harbor diverse heterotrophic bacterial assemblages. While colony-associated microbiomes may influence Microcystis blooms, there remains a limited understanding of the structure and functional potential of these communities and how they may be shaped by changing environmental conditions. To address this gap, we compared the dynamics of Microcystis-attached (MCA), free-living (FL), and whole water (W) microbiomes during Microcystis blooms using next-generation amplicon sequencing (16S rRNA), a predictive metagenome software, and other bioinformatic approaches. Microbiomes were monitored through high resolution spatial-temporal surveys across two North American lakes, Lake Erie (LE) and Lake Agawam (LA; Long Island, NY, United States) in 2017, providing the largest dataset of these fractions to date. Sequencing of 126 samples generated 7,922,628 sequences that clustered into 7,447 amplicon sequence variants (ASVs) with 100% sequence identity. Across lakes, the MCA microbiomes were significantly different than the FL and W fractions being significantly enriched in Gemmatimonadetes, Burkholderiaceae, Rhizobiales, and Cytophagales and depleted of Actinobacteria. Further, although MCA communities harbored > 900 unique ASVs, they were significantly less diverse than the other fractions with diversity inversely related to bloom intensity, suggesting increased selection pressure on microbial communities as blooms intensified. Despite taxonomic differences between lakes, predicted metagenomes revealed conserved functional potential among MCA microbiomes. MCA communities were significantly enriched in pathways involved in N and P cycling and microcystin-degradation. Taxa potentially capable of N2-fixation were significantly enriched (p < 0.05) and up to four-fold more abundant within the MCA faction relative to other fractions, potentially aiding in the proliferation of Microcystis blooms during low N conditions. The MCA predicted metagenomes were conserved over 8 months of seasonal changes in temperature and N availability despite strong temporal succession in microbiome composition. Collectively, these findings indicate that Microcystis colonies harbor a statistically distinct microbiome with a conserved functional potential that may help facilitate bloom persistence under environmentally unfavorable conditions.

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The Composition and Function of Microbiomes Within Microcystis Colonies Are Significantly Different Than Native Bacterial Assemblages in Two North American Lakes

Cyanobacterial carbohydrates, such as sucrose, have been considered as potential renewable feedstock to support the production of fuels and chemicals. However, the separation and purification processes of these carbohydrates will increase the production cost of chemicals. Co-culture fermentation has been proposed as an efficient and economical way to utilize these cyanobacterial carbohydrates. However, studies on the application of co-culture systems to achieve green biosynthesis of platform chemicals are still rare. In this study, we successfully achieved one-step conversion of sucrose derived from cyanobacteria to fine chemicals by constructing a microbial consortium consisting of the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 and Escherichia coli to sequentially produce sucrose and then the platform chemical 3-hydroxypropionic acid (3-HP) from CO2 under photoautotrophic growth conditions. First, efforts were made to overexpress the sucrose permease-coding gene cscB under the strong promoter Pcpc560 in S. elongatus UTEX 2973 for efficient sucrose secretion. Second, the sucrose catabolic pathway and malonyl-CoA-dependent 3-HP biosynthetic pathway were introduced into E. coli BL21 (DE3) for heterologous biosynthesis of 3-HP from sucrose. By optimizing the cultivation temperature from 37 to 30 °C, a stable artificial consortium system was constructed with the capability of producing 3-HP at up to 68.29 mg/L directly from CO2. In addition, cell growth of S. elongatus UTEX 2973 in the consortium was enhanced, probably due to the quick quenching of reactive oxygen species (ROS) in the system by E. coli, which in turn improved the photosynthesis of cyanobacteria. The study demonstrated the feasibility of the one-step conversion of sucrose to fine chemicals using an artificial consortium system. The study also confirmed that heterotrophic bacteria could promote the cell growth of cyanobacteria by relieving oxidative stress in this microbial consortium, which further suggests the potential value of this system for future industrial applications.

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Construction and analysis of an artificial consortium based on the fast-growing cyanobacterium Synechococcus elongatus UTEX 2973 to produce the platform chemical 3-hydroxypropionic acid from CO2

To overcome the limitations associated with studying the interactions between bacterial communities (BCs) and cyanobacteria in natural environments, we compared the structural and functional diversities of the BCs associated with 15 non-axenic cyanobacterial strains in culture and two natural BCs sampled during cyanobacterial blooms. No significant differences in richness and diversity were found between the natural and cultivated BCs, although some of the cyanobacterial strains had been isolated 11 years earlier. Moreover, these BCs shared some similar characteristics, such as a very low abundance of Actinobacteria, but they display significant differences at the operational taxonomic unit (OTU) level. Overall, our findings suggest that BCs associated with cyanobacteria in culture are good models to better understand the interactions between heterotrophic bacteria and cyanobacteria. Additionally, BCs associated with heterocystous cyanobacterial strains cultivated in Z8X culture medium without nitrate (Aphanizomenon-Dolichospermum) demonstrated significant differences compared to BCs associated with non-heterocystous strains cultivated in Z8 culture medium (Planktothrix-Microcystis) in terms of their composition and their ability to utilize different carbon sources, suggesting the potential influence of cyanobacterial metabolism and/or culture media on associated BCs. Finally, half of the dominant OTUs in these BCs were specifically associated with cyanobacteria or other phytoplankton, whereas the remaining OTUs were generally associated with ecosystems containing high organic matter content, such as sludge or intestines.

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Silvia de Cesare

Papers

Bacterial Communities Associated with Four Cyanobacterial Genera Display Structural and Functional Differences: Evidence from an Experimental Approach