scholarly journals Antibiotic production in Streptomyces is organized by a division of labor through terminal genomic differentiation

2020 ◽  
Vol 6 (3) ◽  
pp. eaay5781 ◽  
Author(s):  
Zheren Zhang ◽  
Chao Du ◽  
Frédérique de Barsy ◽  
Michael Liem ◽  
Apostolos Liakopoulos ◽  
...  

One of the hallmark behaviors of social groups is division of labor, where different group members become specialized to carry out complementary tasks. By dividing labor, cooperative groups increase efficiency, thereby raising group fitness even if these behaviors reduce individual fitness. We find that antibiotic production in colonies of Streptomyces coelicolor is coordinated by a division of labor. We show that S. coelicolor colonies are genetically heterogeneous because of amplifications and deletions to the chromosome. Cells with chromosomal changes produce diversified secondary metabolites and secrete more antibiotics; however, these changes reduced individual fitness, providing evidence for a trade-off between antibiotic production and fitness. Last, we show that colonies containing mixtures of mutants and their parents produce significantly more antibiotics, while colony-wide spore production remains unchanged. By generating specialized mutants that hyper-produce antibiotics, streptomycetes reduce the fitness costs of secreted secondary metabolites while maximizing the yield and diversity of these products.

2019 ◽  
Author(s):  
Zheren Zhang ◽  
Frederique de Barsy ◽  
Michael Liem ◽  
Apostolos Liakopoulos ◽  
Young H. Choi ◽  
...  

AbstractOne of the hallmark behaviors of social groups is division of labour, where different group members become specialized to carry out complementary tasks. By dividing labour, cooperative groups of individuals increase their efficiency, thereby raising group fitness even if these specialized behaviors reduce the fitness of individual group members. Here we provide evidence that antibiotic production in colonies of the multicellular bacteriumStreptomyces coelicoloris coordinated by a division of labour. We show thatS. coelicolorcolonies are genetically heterogenous due to massive amplifications and deletions to the chromosome. Cells with gross chromosomal changes produce an increased diversity of secondary metabolites and secrete significantly more antibiotics; however, these changes come at the cost of dramatically reduced individual fitness, providing direct evidence for a trade-off between secondary metabolite production and fitness. Finally, we show that colonies containing mixtures of mutant strains and their parents produce significantly more antibiotics, while colony-wide spore production remains unchanged. Our work demonstrates that by generating mutants that are specialized to hyper-produce antibiotics, streptomycetes reduce the colony-wide fitness costs of secreted secondary metabolites while maximizing the yield and diversity of these products.


2020 ◽  
Author(s):  
Zheren Zhang ◽  
Bart Claushuis ◽  
Dennis Claessen ◽  
Daniel E. Rozen

AbstractIn colonies of the filamentous multicellular bacterium Streptomyces coelicolor, a sub-population of cells arise that hyper-produce metabolically costly antibiotics, resulting in a division of labor that maximizes colony fitness. Because these cells contain large genomic deletions that cause massive reductions to individual fitness, their behavior is altruistic, much like worker castes in eusocial insects. To understand the reproductive and genomic fate of these mutant cells after their emergence, we use experimental evolution by serially transferring populations via spore-to-spore transfer for 25 cycles, reflective of the natural mode of bottlenecked transmission for these spore-forming bacteria. We show that, in contrast to wild-type cells, altruistic mutant cells continue to significantly decline in fitness during transfer while they delete larger and larger fragments from their chromosome ends. In addition, altruistic mutants acquire a roughly 10-fold increase in their base-substitution rates due to mutations in genes for DNA replication and repair. Ecological damage, caused by reduced sporulation, coupled with irreversible DNA damage due to point mutation and deletions, leads to an inevitable and irreversible type of mutational meltdown in these cells. Taken together, these results suggest that the altruistic cells arising in this division of labor are equivalent to reproductively sterile castes of social insects.


2021 ◽  
Author(s):  
Enrico Sandro Colizzi ◽  
Renske MA Vroomans ◽  
Daniel E Rozen ◽  
Roeland M.H. Merks ◽  
Bram van Dijk

Division of labor can evolve when social groups benefit from the functional specialisation of its members. Recently, a novel means of coordinating division of labor was found in the antibiotic-producing bacterium Streptomyces coelicolor, where functionally specialized cells are generated through large-scale genomic re-organisation. Here, we investigate how the evolution of a genome architecture enables such mutation-driven division of labor, using a multi-scale mathematical model of bacterial evolution. We let bacteria compete on the basis of their antibiotic production and growth rate in a spatially structured environment. Bacterial behavior is determined by the structure and composition of their genome, which encodes antibiotics, growth-promoting genes and fragile genomic loci that can induce chromosomal deletions. We find that a genomic organization evolves that partitions growth-promoting genes and antibiotic-coding genes to distinct parts of the genome, separated by fragile genomic loci. Mutations caused by these fragile sites mostly delete growth-promoting genes, generating antibiotic-producing mutants from non-producing (and weakly-producing) progenitors, in agreement with experimental observations. Mutants protect their colony from competitors but are themselves unable to replicate. We further show that this division of labor enhances the local competition between colonies by promoting antibiotic diversity. These results show that genomic organisation can co-evolve with genomic instabilities to enable reproductive division of labor.


eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Robin E Morrison ◽  
Winnie Eckardt ◽  
Fernando Colchero ◽  
Veronica Vecellio ◽  
Tara S Stoinski

Mothers are crucial for mammals’ survival before nutritional independence, but many social mammals reside with their mothers long after. In these species the social adversity caused by maternal loss later in life can dramatically reduce fitness. However, in some human populations these negative consequences can be overcome by care from other group members. We investigated the consequences of maternal loss in mountain gorillas and found no discernible fitness costs to maternal loss through survival, age at first birth, or survival of first offspring through infancy. Social network analysis revealed that relationships with other group members, particularly dominant males and those close in age, strengthened following maternal loss. In contrast to most social mammals, where maternal loss causes considerable social adversity, in mountain gorillas, as in certain human populations, this may be buffered by relationships within cohesive social groups, breaking the link between maternal loss, increased social adversity, and decreased fitness.


2020 ◽  
Author(s):  
Zheren Zhang ◽  
Bart Claushuis ◽  
Dennis Claessen ◽  
Daniel Rozen

Abstract In colonies of the filamentous multicellular bacterium Streptomyces coelicolor, a sub-population of cells arise that hyper-produce metabolically costly antibiotics, resulting in a division of labor that maximizes colony fitness. Because these cells contain large genomic deletions that cause massive reductions to individual fitness, their behavior is altruistic, much like worker castes in eusocial insects. To understand the reproductive and genomic fate of these mutant cells after their emergence, we use experimental evolution by serially transferring populations via spore-to-spore transfer for 25 cycles, reflective of the natural mode of bottlenecked transmission for these spore-forming bacteria. We show that, in contrast to wild-type cells, altruistic mutant cells continue to significantly decline in fitness during transfer while they delete larger and larger fragments from their chromosome ends. In addition, altruistic mutants acquire a roughly 10-fold increase in their base-substitution rates due to mutations in genes for DNA replication and repair. Ecological damage, caused by reduced sporulation, coupled with irreversible DNA damage due to point mutation and deletions, leads to an inevitable and irreversible type of mutational meltdown in these cells. Taken together, these results suggest that the altruistic cells arising in this division of labor are equivalent to reproductively sterile castes of social insects.


Author(s):  
Samuel Bowles ◽  
Herbert Gintis

Why do humans, uniquely among animals, cooperate in large numbers to advance projects for the common good? Contrary to the conventional wisdom in biology and economics, this generous and civic-minded behavior is widespread and cannot be explained simply by far-sighted self-interest or a desire to help close genealogical kin. This book shows that the central issue is not why selfish people act generously, but instead how genetic and cultural evolution has produced a species in which substantial numbers make sacrifices to uphold ethical norms and to help even total strangers. The book describes how, for thousands of generations, cooperation with fellow group members has been essential to survival. Groups that created institutions to protect the civic-minded from exploitation by the selfish flourished and prevailed in conflicts with less cooperative groups. Key to this process was the evolution of social emotions such as shame and guilt, and our capacity to internalize social norms so that acting ethically became a personal goal rather than simply a prudent way to avoid punishment. Using experimental, archaeological, genetic, and ethnographic data to calibrate models of the coevolution of genes and culture as well as prehistoric warfare and other forms of group competition, the book provides a compelling and novel account of human cooperation.


2008 ◽  
Vol 190 (20) ◽  
pp. 6903-6908 ◽  
Author(s):  
Ya-Wen Lu ◽  
Adrianna K. San Roman ◽  
Amy M. Gehring

ABSTRACT The phosphopantetheinyl transferase genes SCO5883 (redU) and SCO6673 were disrupted in Streptomyces coelicolor. The redU mutants did not synthesize undecylprodigiosin, while SCO6673 mutants failed to produce calcium-dependent antibiotic. Neither gene was essential for actinorhodin production or morphological development in S. coelicolor, although their mutation could influence these processes.


2021 ◽  
pp. 095679762110322
Author(s):  
Marcel Montrey ◽  
Thomas R. Shultz

Surprisingly little is known about how social groups influence social learning. Although several studies have shown that people prefer to copy in-group members, these studies have failed to resolve whether group membership genuinely affects who is copied or whether group membership merely correlates with other known factors, such as similarity and familiarity. Using the minimal-group paradigm, we disentangled these effects in an online social-learning game. In a sample of 540 adults, we found a robust in-group-copying bias that (a) was bolstered by a preference for observing in-group members; (b) overrode perceived reliability, warmth, and competence; (c) grew stronger when social information was scarce; and (d) even caused cultural divergence between intermixed groups. These results suggest that people genuinely employ a copy-the-in-group social-learning strategy, which could help explain how inefficient behaviors spread through social learning and how humans maintain the cultural diversity needed for cumulative cultural evolution.


2020 ◽  
Author(s):  
Audam Chhun ◽  
Despoina Sousoni ◽  
Maria del Mar Aguiló-Ferretjans ◽  
Lijiang Song ◽  
Christophe Corre ◽  
...  

AbstractBacteria from the Actinomycete family are a remarkable source of natural products with pharmaceutical potential. The discovery of novel molecules from these organisms is, however, hindered because most of the biosynthetic gene clusters (BGCs) encoding these secondary metabolites are cryptic or silent and are referred to as orphan BGCs. While co-culture has proven to be a promising approach to unlock the biosynthetic potential of many microorganisms by activating the expression of these orphan BGCs, it still remains an underexplored technique. The marine actinobacteria Salinispora tropica, for instance, produces valuable compounds such as the anti-cancer molecule salinosporamide A but half of its putative BGCs are still orphan. Although previous studies have looked into using marine heterotrophs to induce orphan BGCs in Salinispora, the potential impact of co-culturing marine phototrophs with Salinispora has yet to be investigated. Following the observation of clear antimicrobial phenotype of the actinobacterium on a range of phytoplanktonic organisms, we here report the discovery of novel cryptic secondary metabolites produced by S. tropica in response to its co-culture with photosynthetic primary producers. An approach combining metabolomics and proteomics revealed that the photosynthate released by phytoplankton influences the biosynthetic capacities of S. tropica with both production of new molecules and the activation of orphan BGCs. Our work pioneers the use of phototrophs as a promising strategy to accelerate the discovery of novel natural products from actinobacteria.ImportanceThe alarming increase of antimicrobial resistance has generated an enormous interest in the discovery of novel active compounds. The isolation of new microbes to untap novel natural products is currently hampered because most biosynthetic gene clusters (BGC) encoded by these microorganisms are not expressed under standard laboratory conditions, i.e. mono-cultures. Here we show that co-culturing can be an easy way for triggering silent BGC. By combining state-of-the-art metabolomics and high-throughput proteomics, we characterized the activation of cryptic metabolites and silent biosynthetic gene clusters in the marine actinobacteria Salinispora tropica by the presence of phytoplankton photosynthate. We further suggest a mechanistic understanding of the antimicrobial effect this actinobacterium has on a broad range of prokaryotic and eukaryotic phytoplankton species and reveal a promising candidate for antibiotic production.


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