Limits...
Common Cell Shape Evolution of Two Nasopharyngeal Pathogens.

Veyrier FJ, Biais N, Morales P, Belkacem N, Guilhen C, Ranjeva S, Sismeiro O, Péhau-Arnaudet G, Rocha EP, Werts C, Taha MK, Boneca IG - PLoS Genet. (2015)

Bottom Line: Finally, the same evolution was observed for the ancestor of M. catarrhalis.This suggests a strong selection of these genetic events during the colonization of the nasopharynx.This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells.

View Article: PubMed Central - PubMed

Affiliation: Institut Pasteur, Infection Bactériennes Invasives, Département Infection et Epidémiologie, Paris, France; Institut Pasteur, Groupe Biologie et Génétique de la Paroi Bactérienne, Département de Microbiologie, Paris, France; INSERM, Groupe Avenir, Paris, France; INRS-Institut Armand-Frappier, Bacterial Symbionts Evolution, Laval, Quebec, Canada.

ABSTRACT
Respiratory infectious diseases are the third cause of worldwide death. The nasopharynx is the portal of entry and the ecological niche of many microorganisms, of which some are pathogenic to humans, such as Neisseria meningitidis and Moraxella catarrhalis. These microbes possess several surface structures that interact with the actors of the innate immune system. In our attempt to understand the past evolution of these bacteria and their adaption to the nasopharynx, we first studied differences in cell wall structure, one of the strongest immune-modulators. We were able to show that a modification of peptidoglycan (PG) composition (increased proportion of pentapeptides) and a cell shape change from rod to cocci had been selected for along the past evolution of N. meningitidis. Using genomic comparison across species, we correlated the emergence of the new cell shape (cocci) with the deletion, from the genome of N. meningitidis ancestor, of only one gene: yacF. Moreover, the reconstruction of this genetic deletion in a bacterium harboring the ancestral version of the locus together with the analysis of the PG structure, suggest that this gene is coordinating the transition from cell elongation to cell division. Accompanying the loss of yacF, the elongation machinery was also lost by several of the descendants leading to the change in the PG structure observed in N. meningitidis. Finally, the same evolution was observed for the ancestor of M. catarrhalis. This suggests a strong selection of these genetic events during the colonization of the nasopharynx. This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells.

No MeSH data available.


Related in: MedlinePlus

Cell shape evolution among the Neisseriaceae family.Phylogeny of the Neisseriaceae family based on core genome analysis along with scanning electronic microscopy images of representative species or schematic representation of the cell shape based on the literature. The mean total ratio (GM4+GM4_GM4)/(GM5+GM5_GM4) (with standard deviation), assessed by reverse-phase HPLC, is also presented for the lineages having emerged after the different nodes of evolution (*** p≤0.001; ** p≤0.01; * p≤0.05). Each dote represents an independent isolate (tested for rodA presence) from the CNRM collection or from the ATCC collection that have been classified as N. meningitidis (1), N. lactamica (2), N. polysaccharea (1), N. gonorrhoeae (3), N. cinerea (1), N. perflava (1), N. sicca (3), N. subflava (2), N. mucosa (3), N. elongata (1), N. bacilliformis (1), K. oralis (1). Finally, the right part displays the deletions detected at different nodes of evolution by presenting the organization of the different relevant loci in species that diverged before and after the corresponding nodes. Note that the deletion of yacF also occurred in N. wadsworthii suggesting of an independent event at node 3.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4498754&req=5

pgen.1005338.g001: Cell shape evolution among the Neisseriaceae family.Phylogeny of the Neisseriaceae family based on core genome analysis along with scanning electronic microscopy images of representative species or schematic representation of the cell shape based on the literature. The mean total ratio (GM4+GM4_GM4)/(GM5+GM5_GM4) (with standard deviation), assessed by reverse-phase HPLC, is also presented for the lineages having emerged after the different nodes of evolution (*** p≤0.001; ** p≤0.01; * p≤0.05). Each dote represents an independent isolate (tested for rodA presence) from the CNRM collection or from the ATCC collection that have been classified as N. meningitidis (1), N. lactamica (2), N. polysaccharea (1), N. gonorrhoeae (3), N. cinerea (1), N. perflava (1), N. sicca (3), N. subflava (2), N. mucosa (3), N. elongata (1), N. bacilliformis (1), K. oralis (1). Finally, the right part displays the deletions detected at different nodes of evolution by presenting the organization of the different relevant loci in species that diverged before and after the corresponding nodes. Note that the deletion of yacF also occurred in N. wadsworthii suggesting of an independent event at node 3.

Mentions: Bacteria from the Neisseriaceae family have variable cell shape: some are elongated (e.g. Kingella oralis or N. elongata) whereas others present a coccoïd form (e.g. N. meningitidis and N. gonorrhoeae). To establish that these differences were linked to the evolution within the family, we correlated the phylogeny (determined using core genome analysis as described in the M&M) with cell shape verified by scanning electronic microscopy for some representative strains that were received at the Centre National de Reference des Méningocoques or with information found in the literature for other well described strains [12] (Fig 1). Our results suggested that Neisseria cell shape evolved from rod to coccus at a node of evolution that we have called 1 in the Fig 1. As a note, the coccus Neisseria wadsworthii 9715 is related to bacilli Neisseria clade with the closest bacterium being the bacillus Neisseria waeveri. This phylogeny could be biased by a low quality genomic sequence. Nevertheless it is consistent with previous phylogeny (based on the same genomic sequence) [13]. Therefore, this strain may have undergone an independent coccus cell-shape transition.


Common Cell Shape Evolution of Two Nasopharyngeal Pathogens.

Veyrier FJ, Biais N, Morales P, Belkacem N, Guilhen C, Ranjeva S, Sismeiro O, Péhau-Arnaudet G, Rocha EP, Werts C, Taha MK, Boneca IG - PLoS Genet. (2015)

Cell shape evolution among the Neisseriaceae family.Phylogeny of the Neisseriaceae family based on core genome analysis along with scanning electronic microscopy images of representative species or schematic representation of the cell shape based on the literature. The mean total ratio (GM4+GM4_GM4)/(GM5+GM5_GM4) (with standard deviation), assessed by reverse-phase HPLC, is also presented for the lineages having emerged after the different nodes of evolution (*** p≤0.001; ** p≤0.01; * p≤0.05). Each dote represents an independent isolate (tested for rodA presence) from the CNRM collection or from the ATCC collection that have been classified as N. meningitidis (1), N. lactamica (2), N. polysaccharea (1), N. gonorrhoeae (3), N. cinerea (1), N. perflava (1), N. sicca (3), N. subflava (2), N. mucosa (3), N. elongata (1), N. bacilliformis (1), K. oralis (1). Finally, the right part displays the deletions detected at different nodes of evolution by presenting the organization of the different relevant loci in species that diverged before and after the corresponding nodes. Note that the deletion of yacF also occurred in N. wadsworthii suggesting of an independent event at node 3.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4498754&req=5

pgen.1005338.g001: Cell shape evolution among the Neisseriaceae family.Phylogeny of the Neisseriaceae family based on core genome analysis along with scanning electronic microscopy images of representative species or schematic representation of the cell shape based on the literature. The mean total ratio (GM4+GM4_GM4)/(GM5+GM5_GM4) (with standard deviation), assessed by reverse-phase HPLC, is also presented for the lineages having emerged after the different nodes of evolution (*** p≤0.001; ** p≤0.01; * p≤0.05). Each dote represents an independent isolate (tested for rodA presence) from the CNRM collection or from the ATCC collection that have been classified as N. meningitidis (1), N. lactamica (2), N. polysaccharea (1), N. gonorrhoeae (3), N. cinerea (1), N. perflava (1), N. sicca (3), N. subflava (2), N. mucosa (3), N. elongata (1), N. bacilliformis (1), K. oralis (1). Finally, the right part displays the deletions detected at different nodes of evolution by presenting the organization of the different relevant loci in species that diverged before and after the corresponding nodes. Note that the deletion of yacF also occurred in N. wadsworthii suggesting of an independent event at node 3.
Mentions: Bacteria from the Neisseriaceae family have variable cell shape: some are elongated (e.g. Kingella oralis or N. elongata) whereas others present a coccoïd form (e.g. N. meningitidis and N. gonorrhoeae). To establish that these differences were linked to the evolution within the family, we correlated the phylogeny (determined using core genome analysis as described in the M&M) with cell shape verified by scanning electronic microscopy for some representative strains that were received at the Centre National de Reference des Méningocoques or with information found in the literature for other well described strains [12] (Fig 1). Our results suggested that Neisseria cell shape evolved from rod to coccus at a node of evolution that we have called 1 in the Fig 1. As a note, the coccus Neisseria wadsworthii 9715 is related to bacilli Neisseria clade with the closest bacterium being the bacillus Neisseria waeveri. This phylogeny could be biased by a low quality genomic sequence. Nevertheless it is consistent with previous phylogeny (based on the same genomic sequence) [13]. Therefore, this strain may have undergone an independent coccus cell-shape transition.

Bottom Line: Finally, the same evolution was observed for the ancestor of M. catarrhalis.This suggests a strong selection of these genetic events during the colonization of the nasopharynx.This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells.

View Article: PubMed Central - PubMed

Affiliation: Institut Pasteur, Infection Bactériennes Invasives, Département Infection et Epidémiologie, Paris, France; Institut Pasteur, Groupe Biologie et Génétique de la Paroi Bactérienne, Département de Microbiologie, Paris, France; INSERM, Groupe Avenir, Paris, France; INRS-Institut Armand-Frappier, Bacterial Symbionts Evolution, Laval, Quebec, Canada.

ABSTRACT
Respiratory infectious diseases are the third cause of worldwide death. The nasopharynx is the portal of entry and the ecological niche of many microorganisms, of which some are pathogenic to humans, such as Neisseria meningitidis and Moraxella catarrhalis. These microbes possess several surface structures that interact with the actors of the innate immune system. In our attempt to understand the past evolution of these bacteria and their adaption to the nasopharynx, we first studied differences in cell wall structure, one of the strongest immune-modulators. We were able to show that a modification of peptidoglycan (PG) composition (increased proportion of pentapeptides) and a cell shape change from rod to cocci had been selected for along the past evolution of N. meningitidis. Using genomic comparison across species, we correlated the emergence of the new cell shape (cocci) with the deletion, from the genome of N. meningitidis ancestor, of only one gene: yacF. Moreover, the reconstruction of this genetic deletion in a bacterium harboring the ancestral version of the locus together with the analysis of the PG structure, suggest that this gene is coordinating the transition from cell elongation to cell division. Accompanying the loss of yacF, the elongation machinery was also lost by several of the descendants leading to the change in the PG structure observed in N. meningitidis. Finally, the same evolution was observed for the ancestor of M. catarrhalis. This suggests a strong selection of these genetic events during the colonization of the nasopharynx. This selection may have been forced by the requirement of evolving permissive interaction with the immune system, the need to reduce the cellular surface exposed to immune attacks without reducing the intracellular storage capacity, or the necessity to better compete for adhesion to target cells.

No MeSH data available.


Related in: MedlinePlus