Host Specific Diversity in Lactobacillus johnsonii as Evidenced by a Major Chromosomal Inversion and Phage Resistance Mechanisms

Caitriona M Guinane,Colin Hill,Catherine Stanton,Gerald F Fitzgerald,Robert M Kent,R Paul Ross,Sarah Norberg,Sebastien Gagneux

doi:10.1371/journal.pone.0018740

Caitriona M Guinane, Colin Hill + Show 6 more

Open Access

https://doi.org/10.1371/journal.pone.0018740

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Abstract

Genetic diversity and genomic rearrangements are a driving force in bacterial evolution and niche adaptation. We sequenced and annotated the genome of Lactobacillus johnsonii DPC6026, a strain isolated from the porcine intestinal tract. Although the genome of DPC6026 is similar in size (1.97mbp) and GC content (34.8%) to the sequenced human isolate L. johnsonii NCC 533, a large symmetrical inversion of approximately 750 kb differentiated the two strains. Comparative analysis among 12 other strains of L. johnsonii including 8 porcine, 3 human and 1 poultry isolate indicated that the genome architecture found in DPC6026 is more common within the species than that of NCC 533. Furthermore a number of unique features were annotated in DPC6026, some of which are likely to have been acquired by horizontal gene transfer (HGT) and contribute to protection against phage infection. A putative type III restriction-modification system was identified, as were novel Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR) elements. Interestingly, these particular elements are not widely distributed among L. johnsonii strains. Taken together these data suggest intra-species genomic rearrangements and significant genetic diversity within the L. johnsonii species and indicate towards a host-specific divergence of L. johnsonii strains with respect to genome inversion and phage exposure.

Highlights

The Gastro-intestinal (GI) tract is colonized by a vast and diverse community of microbes
This study presents a number of mobile genetic elements (MGE) novel to the L. johnsonii species and previously unidentified phage resistance mechanisms
A novel restriction modification system was annotated on the genome of DPC6026. It is located at,1.57 mbp and consists of a restriction (LJP1436) and a methylase (LJP1437) component typical of the type III family of Restriction Modification (RM) systems (Figure 5b). This type III system has not been previously identified in L. johnsonii and, it does share amino acid identity with the restriction component of L. gasseri (90%) [11] and the modification component of Lactobacillus fermentum (55%) [44], the complete system does not have a close homolog in any sequenced LAB

Summary

Introduction

The Gastro-intestinal (GI) tract is colonized by a vast and diverse community of microbes. Lactobacillus johnsonii is a member of the closely related ‘‘acidophilus complex’’ of lactobacilli and an autochthonous species of the gastro-intestinal tract. For organisms commonly found in GI tract such Lactobacillus acidophilus, Lactobacillus gasseri and L. johnsonii there are a number of genome sequences available which have identified genetic traits that most likely function in gastric survival and promote interactions with the intestinal mucosa [9,10,11,12]. In the L. johnsonii NCC 533 genome for example, large cell surface proteins were identified thought to be involved glycoprotein adhesion and persistence in the intestinal tract [12,14]. Genetic diversity and horizontal gene transfer (HGT) among closely related gut lactobacilli has been observed [11,12,15,16]. This study presents a number of MGE novel to the L. johnsonii species and previously unidentified phage resistance mechanisms

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