Cyanobacterial biofilms are ubiquitous and play important roles in diverse environments, yet, understanding of the processes underlying development of these aggregates is just emerging. Here we report cell specialization in formation of Synechococcus elongatus PCC 7942 biofilms - a hitherto unknown characteristic of cyanobacterial multicellularity. We show that only about a quarter of the cell population expresses at high levels the four-gene ebfG-operon that is required for biofilm formation while almost all cells are present in the biofilm. Detailed characterization of EbfG4 encoded by this operon revealed cell-surface localization as well as its presence in the biofilm matrix. Moreover, EbfG1-3 were shown to form amyloids and are thus likely to contribute to the matrix structure. These data suggest a beneficial division of labour during biofilm formation where only some of the cells allocate resources to produce matrix proteins, public goods that support robust biofilm development by the majority of the cells. Additionally, previous studies revealed the operation of a self-suppression mechanism that depends on an extracellular inhibitor, which supresses transcription of the ebfG-operon. Here we revealed inhibitor activity at an early growth stage and its gradual accumulation along the exponential growth phase in correlation with cell density. Data, however, demonstrate a gradual response to the inhibitor rather than a threshold-like phenomenon known for quorum-sensing in heterotrophs. Together, data presented here demonstrate cell specialization and imply density-dependent regulation thereby providing novel insights into cyanobacterial communal behaviour.
Biotic and abiotic interactions shape natural microbial communities. The mechanisms behind microbe-microbe interactions, particularly those protein-based, are not well understood. We hypothesize that secreted proteins are a powerful and highly specific toolset to shape and defend plant niches. We have studied Albugo candida, an obligate plant parasite from the protist Oomycota phylum, for its potential to modulate the growth of bacteria through secretion of proteins into the apoplast. Amplicon sequencing and network analysis of Albugo-infected and uninfected samples revealed an abundance of negative correlations between Albugo and other phyllosphere microbes. Analysis of the apoplastic proteome of Albugo colonized leaves combined with machine-learning predictors enabled the selection of candidates for heterologous expression and study of their inhibitory activity. We found that three of the candidate proteins show selective antimicrobial activity on gram-positive bacteria isolated from Arabidopsis thaliana and that these inhibited bacteria are important for the stability of the community structure. We could ascribe the antibacterial activity of the candidates to intrinsically disordered regions and positively correlate it with net charge. This is the first report of protist proteins with antimicrobial activity under apoplastic conditions that therefore are potential biocontrol tools for targeted manipulations of the microbiome.
Amyloids have proven to be a widespread phenomenon rather than an exception. Many proteins presenting the hallmarks of this characteristic beta sheet-rich folding have been described to date. Particularly common are functional amyloids that play an important role in the promotion of survival and pathogenicity in prokaryotes. Here, we describe important developments in amyloid protein research that relate to microbe-microbe and microbe-host interactions in the plant microbiome. Starting with biofilms, which are a broad strategy for bacterial persistence that is extremely important for plant colonization. Microbes rely on amyloid-based mechanisms to adhere and create a protective coating that shelters them from external stresses and promotes cooperation. Another strategy generally carried out by amyloids is the formation of hydrophobic surface layers. Known as hydrophobins, these proteins coat the aerial hyphae and spores of plant pathogenic fungi, as well as certain bacterial biofilms. They contribute to plant virulence through promoting dissemination and infectivity. Furthermore, antimicrobial activity is an interesting outcome of the amyloid structure that has potential application in medicine and agriculture. There are many known antimicrobial amyloids released by animals and plants; however, those produced by bacteria or fungi remain still largely unknown. Finally, we discuss amyloid proteins with a more indirect mode of action in their host interactions. These include virulence-promoting harpins, signaling transduction that functions through amyloid templating, and root nodule bacteria proteins that promote plant-microbe symbiosis. In summary, amyloids are an interesting paradigm for their many functional mechanisms linked to bacterial survival in plant-associated microbial communities.
Summary Biotic and abiotic interactions shape natural microbial communities. The mechanisms behind microbe–microbe interactions, particularly those protein based, are not well understood. We hypothesize that released proteins with antimicrobial activity are a powerful and highly specific toolset to shape and defend plant niches. We have studied Albugo candida, an obligate plant parasite from the protist Oomycota phylum, for its potential to modulate the growth of bacteria through release of antimicrobial proteins into the apoplast. Amplicon sequencing and network analysis of Albugo‐infected and uninfected wild Arabidopsis thaliana samples revealed an abundance of negative correlations between Albugo and other phyllosphere microbes. Analysis of the apoplastic proteome of Albugo‐colonized leaves combined with machine learning predictors enabled the selection of antimicrobial candidates for heterologous expression and study of their inhibitory function. We found for three candidate proteins selective antimicrobial activity against Gram‐positive bacteria isolated from A. thaliana and demonstrate that these inhibited bacteria are precisely important for the stability of the community structure. We could ascribe the antibacterial activity of the candidates to intrinsically disordered regions and positively correlate it with their net charge. This is the first report of protist proteins with antimicrobial activity under apoplastic conditions that therefore are potential biocontrol tools for targeted manipulation of the microbiome.
As evidenced in parasitism, host and niche shifts are a source of genomic and phenotypic diversification. Exemplary is a reduction in the core metabolism as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversification. However, selective pressures acting on the genome of organisms that have undergone recent lifestyle or host changes have not been fully investigated. Here, we developed a comparative genomics approach to study underlying adaptive trends in oomycetes, a eukaryotic phylum with a wide and diverse range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes that have similar lifestyles. Moreover, we find that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaptation in oomycetes. Given the high correlation between lifestyle and genome properties in our oomycete dataset, together with the known convergent evolution of fungal and oomycete genomes, we developed a model that predicts plant pathogenic lifestyles with high accuracy based on functional annotations. These insights into how selective pressures correlate with lifestyle may be crucial to better understand host/lifestyle shifts and their impact on the genome.
Cyanobacterial biofilms are ubiquitous and play important roles in diverse environments, yet, understanding of the processes underlying the development of these aggregates is just emerging. Here we report cell specialization in formation of Synechococcus elongatus PCC 7942 biofilms—a hitherto unknown characteristic of cyanobacterial social behavior. We show that only a quarter of the cell population expresses at high levels the four-gene ebfG-operon that is required for biofilm formation. Almost all cells, however, are assembled in the biofilm. Detailed characterization of EbfG4 encoded by this operon revealed cell-surface localization as well as its presence in the biofilm matrix. Moreover, EbfG1-3 were shown to form amyloid structures such as fibrils and are thus likely to contribute to the matrix structure. These data suggest a beneficial ‘division of labor’ during biofilm formation where only some of the cells allocate resources to produce matrix proteins—‘public goods’ that support robust biofilm development by the majority of the cells. In addition, previous studies revealed the operation of a self-suppression mechanism that depends on an extracellular inhibitor, which supresses transcription of the ebfG-operon. Here we revealed inhibitor activity at an early growth stage and its gradual accumulation along the exponential growth phase in correlation with cell density. Data, however, do not support a threshold-like phenomenon known for quorum-sensing in heterotrophs. Together, data presented here demonstrate cell specialization and imply density-dependent regulation thereby providing deep insights into cyanobacterial communal behavior.
BackgroundHost and niche shifts are a source of genomic and phenotypic diversification as evidenced in parasitism. Most characteristic is core metabolism reduction as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversification. However, selective pressures acting on the genome of such organisms are not fully understood.ResultsHere, we developed a comparative genomic approach to study underlying adaptive trends in oomycetes, a eukaryote phylum with a broad range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes inhabiting similar niches. We find that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaption in oomycetes.DiscussionGiven the high correlation of lifestyle to genome properties in our oomycete dataset and the convergent evolution of fungal and oomycete genomes, we have developed a model that predicts plant pathogen lifestyles with high accuracy. Understanding how genomes and selective pressures correlate with lifestyle may be crucial to identify new emerging diseases and pandemic threats.
Background: Host and niche shifts are a source of genomic and phenotypic diversi_cation as evidenced in parasitism. Most characteristic is core metabolism reduction as parasites adapt to a particular host, while the accessory genome often maintains a high degree of diversi_cation. However, selective pressures acting on the genome of such organisms are not fully understood. Results: Here, we developed a comparative genomic approach to study underlying adaptive trends in oomycetes, a eukaryotic phylum with a broad range of economically important plant and animal parasitic lifestyles. Our analysis reveals converging evolution on biological processes for oomycetes inhabiting similar niches. We _nd that certain functions, in particular carbohydrate metabolism, transport, and signaling, are important for host and environmental adaption in oomycetes. Discussion: Given the high correlation of lifestyle to genome properties in our oomycete dataset and the convergent evolution of fungal and oomycete genomes, we have developed a model that predicts plant pathogen lifestyles with high accuracy. Understanding how genomes and selective pressures correlate with lifestyle may be crucial to identify new emerging diseases and pandemic threats.
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