scholarly journals Slightly beneficial genes are retained by bacteria evolving DNA uptake despite selfish elements

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Bram van Dijk ◽  
Paulien Hogeweg ◽  
Hilje M Doekes ◽  
Nobuto Takeuchi

Horizontal gene transfer (HGT) and gene loss result in rapid changes in the gene content of bacteria. While HGT aids bacteria to adapt to new environments, it also carries risks such as selfish genetic elements (SGEs). Here, we use modelling to study how HGT of slightly beneficial genes impacts growth rates of bacterial populations, and if bacterial collectives can evolve to take up DNA despite selfish elements. We find four classes of slightly beneficial genes: indispensable, enrichable, rescuable, and unrescuable genes. Rescuable genes — genes with small fitness benefits that are lost from the population without HGT — can be collectively retained by a community that engages in costly HGT. While this ‘gene-sharing’ cannot evolve in well-mixed cultures, it does evolve in a spatial population like a biofilm. Despite enabling infection by harmful SGEs, the uptake of foreign DNA is evolutionarily maintained by the hosts, explaining the coexistence of bacteria and SGEs.

2020 ◽  
Author(s):  
B. van Dijk ◽  
P. Hogeweg ◽  
H.M. Doekes ◽  
N. Takeuchi

AbstractHorizontal gene transfer (HGT) is a key component of bacterial evolution, which in concert with gene loss can result in rapid changes in gene content. While HGT can evidently aid bacteria to adapt to new environments, it also carries risks since bacteria may pick up selfish genetic elements (SGEs). Here, we use modeling to study how bacterial growth rates are affected by HGT of slightly beneficial genes, if bacteria can evolve HGT to improve their growth rates, and when HGT is evolutionarily maintained in light of harmful SGEs. We find that we can distinguish between four classes of slightly beneficial genes: indispensable, enrichable, rescuable, and unrescuable genes. Rescuable genes – genes that confer small fitness benefits and are lost from the population in the absence of HGT — can be collectively retained by a bacterial community that engages in HGT. While this ‘gene-sharing’ cannot evolve in well-mixed cultures, it does evolve in a spatially structured population such as a biofilm. Although HGT does indeed enable infection by harmful SGEs, HGT is nevertheless evolutionarily maintained by the hosts, explaining the stable coexistence and co-evolution of bacteria and SGEs.


Genetics ◽  
2020 ◽  
Vol 216 (2) ◽  
pp. 543-558
Author(s):  
Shai Slomka ◽  
Itamar Françoise ◽  
Gil Hornung ◽  
Omer Asraf ◽  
Tammy Biniashvili ◽  
...  

Tracing evolutionary processes that lead to fixation of genomic variation in wild bacterial populations is a prime challenge in molecular evolution. In particular, the relative contribution of horizontal gene transfer (HGT) vs.de novo mutations during adaptation to a new environment is poorly understood. To gain a better understanding of the dynamics of HGT and its effect on adaptation, we subjected several populations of competent Bacillus subtilis to a serial dilution evolution on a high-salt-containing medium, either with or without foreign DNA from diverse pre-adapted or naturally salt tolerant species. Following 504 generations of evolution, all populations improved growth yield on the medium. Sequencing of evolved populations revealed extensive acquisition of foreign DNA from close Bacillus donors but not from more remote donors. HGT occurred in bursts, whereby a single bacterial cell appears to have acquired dozens of fragments at once. In the largest burst, close to 2% of the genome has been replaced by HGT. Acquired segments tend to be clustered in integration hotspots. Other than HGT, genomes also acquired spontaneous mutations. Many of these mutations occurred within, and seem to alter, the sequence of flagellar proteins. Finally, we show that, while some HGT fragments could be neutral, others are adaptive and accelerate evolution.


2020 ◽  
Vol 66 (6) ◽  
pp. 1069-1071
Author(s):  
Bram van Dijk

Abstract Bacteria and other prokaryotes evolve primarily through rapid changes in their gene content by quickly losing and gaining genes whenever an ecological opportunity emerges. As gene loss and horizontal gene transfer (HGT) appear to be the most common events across the prokaryotic tree of life, we need to think beyond gradual sequence evolution if we wish to understand the microbial world. Especially genes that reside on mobile genetic elements (MGEs) may spread much more rapidly through a microbial population than genes that reside on the bacterial chromosome. This raises the question: why are some genes associated with MGEs, while others are not? Here, I briefly review a recently proposed class of genes for which we have coined the term “rescuable genes”. The fitness effect of carrying these genes is so small, either constantly or on average, that they are prone to be lost from a microbial population. I argue that HGT, even when costly to the individual cells, may play an important role in maintaining these rescuable genes in microbial communities.


2021 ◽  
Vol 12 (1) ◽  
Author(s):  
David Moreira ◽  
Yvan Zivanovic ◽  
Ana I. López-Archilla ◽  
Miguel Iniesto ◽  
Purificación López-García

AbstractThe Candidate Phyla Radiation (CPR) constitutes a large group of mostly uncultured bacterial lineages with small cell sizes and limited biosynthetic capabilities. They are thought to be symbionts of other organisms, but the nature of this symbiosis has been ascertained only for cultured Saccharibacteria, which are epibiotic parasites of other bacteria. Here, we study the biology and the genome of Vampirococcus lugosii, which becomes the first described species of Vampirococcus, a genus of epibiotic bacteria morphologically identified decades ago. Vampirococcus belongs to the CPR phylum Absconditabacteria. It feeds on anoxygenic photosynthetic gammaproteobacteria, fully absorbing their cytoplasmic content. The cells divide epibiotically, forming multicellular stalks whose apical cells can reach new hosts. The genome is small (1.3 Mbp) and highly reduced in biosynthetic metabolism genes, but is enriched in genes possibly related to a fibrous cell surface likely involved in interactions with the host. Gene loss has been continuous during the evolution of Absconditabacteria, and generally most CPR bacteria, but this has been compensated by gene acquisition by horizontal gene transfer and de novo evolution. Our findings support parasitism as a widespread lifestyle of CPR bacteria, which probably contribute to the control of bacterial populations in diverse ecosystems.


2001 ◽  
Vol 12 (3) ◽  
pp. 217-243 ◽  
Author(s):  
D.G. Cvitkovitch

The oral streptococci are normally non-pathogenic residents of the human microflora. There is substantial evidence that these bacteria can, however, act as "genetic reservoirs" and transfer genetic information to transient bacteria as they make their way through the mouth, the principal entry point for a wide variety of bacteria. Examples that are of particular concern include the transfer of antibiotic resistance from oral streptococci to Streptococcus pneumoniae. The mechanisms that are used by oral streptococci to exchange genetic information are not well-understood, although several species are known to enter a physiological state of genetic competence. This state permits them to become capable of natural genetic transformation, facilitating the acquisition of foreign DNA from the external environment. The oral streptococci share many similarities with two closely related Gram-positive bacteria. S. pneumoniae and Bacillus subtilis. In these bacteria, the mechanisms of quorum-sensing, the development of competence, and DNA uptake and integration are well-charaterized. Using this knowledge and the data available in genome databases allowed us to identify putative genes involved in these processes in the oral organism Streptococcus mutans. Models of competence development and genetic transformation in the oral streptococci and strategies to confirm these models are discussed. Future studies of competence in oral biofilms, the natural environment of oral streptococci, will be discussed.


2016 ◽  
Vol 7 ◽  
Author(s):  
Sophie R. Ullrich ◽  
Carolina González ◽  
Anja Poehlein ◽  
Judith S. Tischler ◽  
Rolf Daniel ◽  
...  

2020 ◽  
Vol 202 (24) ◽  
Author(s):  
Emily M. Kibby ◽  
Aaron T. Whiteley

ABSTRACT The arms race between bacteria and their competitors has produced an astounding variety of conflict systems that are shared via horizontal gene transfer across bacterial populations. In this issue of the Journal of Bacteriology, Burroughs and Aravind investigate how these biological conflict systems have been mixed and matched into new configurations, often with novel protein domains (A. M. Burroughs and L. Aravind, J Bacteriol 202:e00365-20, 2020, https://doi.org/10.1128/JB.00365-20). The authors additionally characterize the evolutionary history of genes in eukaryotes that appear to have been acquired from these prokaryotic defense systems.


Author(s):  
Piyush Behari Lal ◽  
Fritz Wells ◽  
Kevin S. Myers ◽  
Rajdeep Banerjee ◽  
Adam M. Guss ◽  
...  

Zymomonas mobilis has emerged as a promising candidate for production of high value bioproducts from plant biomass. However, a major limitation in equipping Z. mobilis with novel pathways to achieve this goal is restriction of heterologous DNA. Here, we characterized the contribution of several defense systems of Z. mobilis strain ZM4 to impeding heterologous gene transfer from an Escherichia coli donor. Bioinformatic analysis revealed that Z. mobilis ZM4 encodes a previously described mrr -like Type IV Restriction Modification (RM) system, a Type I-F CRISPR system, a chromosomal Type I RM ( hsdMS c ) and a previously uncharacterized Type I RM system, located on an endogenous plasmid ( hsdRMS p ). The DNA recognition motif of HsdRMS p was identified by comparing the methylated DNA sequence pattern of mutants lacking one or both of the hsdMS c and hsdRMS p systems to the parent strain. The conjugation efficiency of synthetic plasmids containing single or combinations of the HsdMS c and HsdRMS p recognition sites indicated that both systems are active and decrease uptake of foreign DNA. In contrast, deletions of mrr and cas3 led to no detectable improvement in conjugation efficiency for the exogenous DNA tested. Thus, the suite of markerless restriction - strains that we constructed, and the knowledge of this new restriction system and its DNA recognition motif provide the necessary platform to flexibly engineer the next generation of Z. mobilis strains for synthesis of valuable products. Importance Zymomonas mobilis is equipped with a number of traits that make it a desirable platform organism for metabolic engineering to produce valuable bioproducts. Engineering strains equipped with synthetic pathways for biosynthesis of new molecules requires integration of foreign genes. In this study we have developed an all-purpose strain, devoid of known host restriction systems and free of any antibiotic resistance markers, which dramatically improves the uptake efficiency of heterologous DNA into Z. mobilis ZM4. We also confirmed the role of a previously known restriction system as well as identified a previously unknown Type I RM system on an endogenous plasmid. Elimination of the barriers to DNA uptake as shown here will allow facile genetic engineering of Z. mobilis .


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