ABSTRACT The frequency and intensity of cyanobacterial blooms are increasing worldwide. Interactions between toxic cyanobacteria and aquatic microorganisms need to be critically evaluated to understand microbial drivers and modulators of the blooms. In this study, we applied 16S/18S rRNA gene sequencing and metabolomics analyses to measure the microbial community composition and metabolic responses of the cyanobacterium Microcystis aeruginosa in a coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to representative concentrations in Lake Taihu, China. M. aeruginosa secreted alkaline phosphatase using a DIP source produced by moribund and decaying microorganisms when the P source was insufficient. During this process, M. aeruginosa accumulated several intermediates in energy metabolism pathways to provide energy for sustained high growth rates and increased intracellular sugars to enhance its competitive capacity and ability to defend itself against microbial attack. It also produced a variety of toxic substances, including microcystins, to inhibit metabolite formation via energy metabolism pathways of aquatic microorganisms, leading to a negative effect on bacterial and eukaryotic microbial richness and diversity. Overall, compared with the monoculture system, the growth of M. aeruginosa was accelerated in coculture, while the growth of some cooccurring microorganisms was inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. These findings provide valuable information for clarifying how M. aeruginosa can potentially modulate its associations with other microorganisms, with ramifications for its dominance in aquatic ecosystems. IMPORTANCE We measured the microbial community composition and metabolic responses of Microcystis aeruginosa in a microcosm coculture system receiving dissolved inorganic nitrogen and phosphorus (DIP) close to the average concentrations in Lake Taihu. In the coculture system, DIP is depleted and the growth and production of aquatic microorganisms can be stressed by a lack of DIP availability. M. aeruginosa could accelerate its growth via interactions with specific cooccurring microorganisms and the accumulation of several intermediates in energy metabolism-related pathways. Furthermore, M. aeruginosa can decrease the carbohydrate metabolism of cooccurring aquatic microorganisms and thus disrupt microbial activities in the coculture. This also had a negative effect on bacterial and eukaryotic microbial richness and diversity. Microcystin was capable of decreasing the biomass of total phytoplankton in aquatic microcosms. Overall, compared to the monoculture, the growth of total aquatic microorganisms is inhibited, with the diversity and richness of eukaryotic microorganisms being more negatively impacted than those of prokaryotic microorganisms. The only exception is M. aeruginosa in the coculture system, whose growth was accelerated.
more »
« less
Nutrient Loading and Viral Memory Drive Accumulation of Restriction Modification Systems in Bloom-Forming Cyanobacteria
ABSTRACT The mechanisms driving cyanobacterial harmful algal blooms (HABs) like those caused by Microcystis aeruginosa remain elusive, but improved defense against viral predation has been implicated for success in eutrophic environments. Our genus-level analyses of 139,023 genomes revealed that HAB-forming cyanobacteria carry vastly more restriction modification systems per genome (RMPG) than nearly all other prokaryotic genera, suggesting that viral defense is a cornerstone of their ecological success. In contrast, picocyanobacteria that numerically dominate nutrient-poor systems have the fewest RMPG within the phylum Cyanobacteria . We used classic resource competition models to explore the hypothesis that nutrient enrichments drive ecological selection for high RMPG due to increased host-phage contact rate. These classic models, agnostic to the mechanism of defense, explain how nutrient loading can select for increased RMPG but, importantly, fail to explain the extreme accumulation of these defense systems. However, extreme accumulation of RMPG can be achieved in a novel “memory” model that accounts for a unique activity of restriction modification systems: the accidental methylation of viral DNA by the methyltransferase. The methylated virus “remembers” the RM defenses of its former host and can evade these defenses if they are present in the next host. This viral memory leads to continual RM system devaluation; RMs accumulate extensively because the benefit of each addition is diminished. Our modeling leads to the hypothesis that nutrient loading and virion methylation drive the extreme accumulation of RMPG in HAB-forming cyanobacteria. Finally, our models suggest that hosts with different RMPG values can coexist when hosts have unique sets of RM systems. IMPORTANCE Harmful algal blooms (HABs), caused by cyanobacteria like Microcystis aeruginosa , are a global threat to water quality and use across the planet. Researchers have agreed that nutrient loading is a major contributor to HAB persistence. While we may understand the environmental conditions that cause HABs, we still struggle in identifying the mechanisms that explain why these organisms have a competitive edge against other, less ecologically hazardous organisms. Our interdisciplinary approach in microbiology, mathematical population modeling, and genomics allows us to use nearly 70 years of research in restriction modification systems to show that HAB-forming cyanobacteria are exceptional in their ability to defend against viruses, and this capacity is intimately tied to nutrient loading. Our hypothesis suggests that defense against viral predation is a fundamental pillar of cyanobacterial ecological strategy and an important contributor to HAB dynamics.
more »
« less
- Award ID(s):
- 1840715
- NSF-PAR ID:
- 10275084
- Editor(s):
- Moran, Mary Ann
- Date Published:
- Journal Name:
- mBio
- Volume:
- 12
- Issue:
- 3
- ISSN:
- 2150-7511
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Humbert, Jean-François (Ed.)Microbial interactions in harmful algal bloom (HAB) communities have been examined in marine systems, but are poorly studied in fresh waters. To investigate HAB-microbe interactions, we isolated bacteria with close associations to bloom-forming cyanobacteria, Microcystis spp., during a 2017 bloom in the western basin of Lake Erie. The genomes of five isolates ( Exiguobacterium sp. JMULE1, Enterobacter sp. JMULE2, Deinococcus sp. JMULE3, Paenibacillus sp. JMULE4, and Acidovorax sp. JMULE5.) were sequenced on a PacBio Sequel system. These genomes ranged in size from 3.1 Mbp ( Exiguobacterium sp. JMULE1) to 5.7 Mbp ( Enterobacter sp. JMULE2). The genomes were analyzed for genes relating to critical metabolic functions, including nitrogen reduction and carbon utilization. All five of the sequenced genomes contained genes that could be used in potential signaling and nutrient exchange between the bacteria and cyanobacteria such as Microcystis . Gene expression signatures of algal-derived carbon utilization for two isolates were identified in Microcystis blooms in Lake Erie and Lake Tai ( Taihu ) at low levels, suggesting these organisms are active and may have a functional role during Microcystis blooms in aggregates, but were largely missing from whole water samples. These findings build on the growing evidence that the bacterial microbiome associated with bloom-forming algae have the functional potential to contribute to nutrient exchange within bloom communities and interact with important bloom formers like Microcystis .more » « less
-
Nojiri, Hideaki (Ed.)ABSTRACT In the oligotrophic oceans, key autotrophs depend on “helper” bacteria to reduce oxidative stress from hydrogen peroxide (H 2 O 2 ) in the extracellular environment. H 2 O 2 is also a ubiquitous stressor in freshwaters, but the effects of H 2 O 2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H 2 O 2 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 H 2 O 2 concentrations and the microbes responsible for H 2 O 2 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 H 2 O 2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H 2 O 2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H 2 O 2 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 H 2 O 2 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 (H 2 O 2 ) 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 H 2 O 2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H 2 O 2 by associated heterotrophic bacteria, which may impact bloom development.more » « less
-
Humbert, Jean-François (Ed.)Harmful algal blooms are commonly thought to be dominated by a single genus, but they are not homogenous communities. Current approaches, both molecular and culture-based, often overlook fine-scale variations in community composition that can influence bloom dynamics. We combined homology-based searches (BLASTX) and phylogenetics to distinguish and quantify Microcystis host and phage members across a summer season during a 2014 Microcystis- dominated bloom that occurred in Lake Tai ( Taihu ), China. We found 47 different genotypes of the Microcystis- specific DNA-dependent RNA polymerase ( rpo B), which included several morphospecies. Microcystis flos-aquae and Microcystis wesenbergii accounted for ~86% of total Microcystis transcripts, while the more commonly studied Microcystis aeruginosa only accounted for ~7%. Microcystis genotypes were classified into three temporal groups according to their expression patterns across the course of the bloom: early, constant and late. All Microcystis morphospecies were present in each group, indicating that expression patterns were likely dictated by competition driven by environmental factors, not phylogeny. We identified three primary Microcystis -infecting phages based on the viral terminase, including a novel Siphoviridae phage that may be capable of lysogeny. Within our dataset, Myoviridae phages consistent with those infecting Microcystis in a lytic manner were positively correlated to the early host genotypes, while the Siphoviridae phages were positively correlated to the late host genotypes, when the Myoviridae phages express putative genetic markers for lysogeny. The expression of genes in the microcystin-encoding mcy cassette was estimated using mcyA , which revealed 24 Microcystis- specific genotypes that were negatively correlated to the early host genotypes. Of all environmental factors measured, pH best described the temporal shift in the Microcystis community genotypic composition, promoting hypotheses regarding carbon concentration mechanisms and oxidative stress. Our work expounds on the complexity of HAB events, using a well-studied dataset to highlight the need for increased resolution of community dynamics.more » « less
-
more » « less
Abstract Intraspecific niche divergence is an important driver of species range, population abundance and impacts on ecosystem functions. Genetic changes are the primary focus when studying intraspecific divergence; however, the role of ecological interactions, particularly host‐microbiome symbioses, is receiving increased attention. The relative importance of these evolutionary and ecological mechanisms has seen only limited evaluation. To address this question, we used
Microcystis aeruginosa , the globally distributed cyanobacterium that dominates freshwater harmful algal blooms. These blooms have been increasing in occurrence and intensity worldwide, causing major economic and ecological damages. We evaluated 46 isolates ofM. aeruginosa and their microbiomes, collected from 14 lakes in Michigan, USA, that vary over 20‐fold in phosphorus levels, the primary limiting nutrient in freshwater systems. Genomes ofM. aeruginosa diverged along this phosphorus gradient in genomic architecture and protein functions. Fitness in low‐phosphorus lakes corresponded with additional shifts withinM. aeruginosa including genome‐wide reductions in nitrogen use, an expansion of phosphorus assimilation genes and an alternative life history strategy of nonclonal colony formation. In addition to host shifts, despite culturing in common‐garden conditions, host‐microbiomes diverged along the gradient in taxonomy, but converged in function with evidence of metabolic interdependence between the host and its microbiome. Divergence corresponded with a physiological trade‐off between fitness in low‐phosphorus environments and growth rate in phosphorus‐rich conditions. Co‐occurrence of genotypes adapted to different nutrient environments in phosphorus‐rich lakes may have critical implications for understanding howM. aeruginosa blooms persist after initial nutrient depletion. Ultimately, we demonstrate that the intertwined effects of genome evolution, host life history strategy and ecological interactions between a host and its microbiome correspond with an intraspecific niche shift with important implications for whole ecosystem function.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1128/mBio.00873-21
