The extracellular proteome of two Bifidobacterium species reveals different adaptation strategies to low iron conditions

Vazquez-Gutierrez, Pamela; Stevens, Marc J. A.; Gehrig, Peter; Barkow-Oesterreicher, Simon; Lacroix, Christophe; Chassard, Christophe

doi:10.1186/s12864-016-3472-x

Cited by 13 publications

(9 citation statements)

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“…Non-closed pan-genomes are typical for heterogeneous datasets, like the Lactobacillus dataset in this study, for species with diverse habitats, like L. plantarum in this study , and in species with high acquisition of genes, such as natural competent streptococci [ 16 , 21 ]. Acquisition of genes occurs in lactobacilli occurs via HGT, which parallels observations in another genus frequently associated with the human gut: Bifidobacteria [ 43 ].…”

Section: Discussionmentioning

confidence: 69%

Clustering of Pan- and Core-genome of Lactobacillus provides Novel Evolutionary Insights for Differentiation

2018

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BackgroundBacterial taxonomy aims to classify bacteria based on true evolutionary events and relies on a polyphasic approach that includes phenotypic, genotypic and chemotaxonomic analyses. Until now, complete genomes are largely ignored in taxonomy. The genus Lactobacillus consists of 173 species and many genomes are available to study taxonomy and evolutionary events.ResultsWe analyzed and clustered 98 completely sequenced genomes of the genus Lactobacillus and 234 draft genomes of 5 different Lactobacillus species, i.e. L. reuteri, L. delbrueckii, L. plantarum, L. rhamnosus and L. helveticus. The core-genome of the genus Lactobacillus contains 266 genes and the pan-genome 20′800 genes. Clustering of the Lactobacillus pan- and core-genome resulted in two highly similar trees. This shows that evolutionary history is traceable in the core-genome and that clustering of the core-genome is sufficient to explore relationships. Clustering of core- and pan-genomes at species’ level resulted in similar trees as well. Detailed analyses of the core-genomes showed that the functional class “genetic information processing” is conserved in the core-genome but that “signaling and cellular processes” is not. The latter class encodes functions that are involved in environmental interactions. Evolution of lactobacilli seems therefore directed by the environment. The type species L. delbrueckii was analyzed in detail and its pan-genome based tree contained two major clades whose members contained different genes yet identical functions. In addition, evidence for horizontal gene transfer between strains of L. delbrueckii, L. plantarum, and L. rhamnosus, and between species of the genus Lactobacillus is presented. Our data provide evidence for evolution of some lactobacilli according to a parapatric-like model for species differentiation.ConclusionsCore-genome trees are useful to detect evolutionary relationships in lactobacilli and might be useful in taxonomic analyses. Lactobacillus’ evolution is directed by the environment and HGT.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4601-5) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 69%

Clustering of Pan- and Core-genome of Lactobacillus provides Novel Evolutionary Insights for Differentiation

2018

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“…The other gene of the operon (LMG13195_RS01880) was also upregulated in coculture and encodes a protein annotated as an amino acid ABC transporter substrate-binding protein with a domain related to iron transport (Fe 2ϩ transport protein). Iron permease genes have been detected in B. breve and Bifidobacterium pseudolongum, as well as in B. bifidum strains, and their expression is increased in iron-limited conditions (31)(32)(33). Several genes involved in nucleotide transport and metabolism were downregulated in coculture ( Fig.…”

Section: Discussionmentioning

confidence: 96%

Bifidobacterium bifidum ATCC 15696 and Bifidobacterium breve 24b Metabolic Interaction Based on 2′- O -Fucosyl-Lactose Studied in Steady-State Cultures in a Freter-Style Chemostat

Centanni

Ferguson

Sims

et al. 2019

Appl Environ Microbiol

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Infants fed breast milk harbor a gut microbiota in which bifidobacteria are generally predominant. The metabolic interactions of bifidobacterial species need investigation because they may offer insight into the colonization of the gut in early life.Bifidobacterium bifidumATCC 15696 hydrolyzes 2′-O-fucosyl-lactose (2FL; a major fucosylated human milk oligosaccharide) but does not use fucose released into the culture medium. However, fucose is a growth substrate forBifidobacterium breve24b, and both strains utilize lactose for growth. The provision of fucose and lactose byB. bifidum(the donor) allowing the growth ofB. breve(the beneficiary) conforms to the concept of syntrophy, but both strains will compete for lactose to multiply. To determine the metabolic impact of this syntrophic/competitive relationship on the donor, the transcriptomes ofB. bifidumwere determined and compared in steady-state monoculture and coculture using transcriptome sequencing (RNA-seq) and reverse transcription-quantitative PCR (RT-qPCR).B. bifidumgenes upregulated in coculture included those encoding alpha-l-fucosidase and carbohydrate transporters and those involved in energy production and conversion.B. bifidumabundance was the same in coculture as in monoculture, butB. brevedominated the coculture numerically. Cocultures during steady-state growth in 2FL medium produced mostly acetate with little lactate (acetate:lactate molar ratio, 8:1) compared to that in monobatch cultures containing lactose (2:1), which reflected the maintenance of steady-state cells in log-phase growth. Darwinian competition is an implicit feature of bacterial communities, but syntrophy is a phenomenon putatively based on cooperation. Our results suggest that the regulation of syntrophy, in addition to competition, may shape bacterial communities.IMPORTANCEThis study addresses the microbiology and function of a natural ecosystem (the infant bowel) usingin vitroexperimentation with bacterial cultures maintained under controlled growth and environmental conditions. We studied the growth of bifidobacteria whose nutrition centered on the hydrolysis of a human milk oligosaccharide. The results revealed responses relating to metabolism occurring in aBifidobacterium bifidumstrain when it provided nutrients that allowed the growth ofBifidobacterium breve, and so discovered biochemical features of these bifidobacteria in relation to metabolic interaction in the shared environment. These kinds of experiments are essential in developing concepts of bifidobacterial ecology that relate to the development of the gut microbiota in early life.

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“…A recent study carried out by Vazquez-Gutierrez et al identified a number of iron uptake clusters utilising a proteomic approach, this analysis identified three ferrous iron transporters in the secretome of B. kashiwanohense PV20-2: AH68_00590 and AH68_00595 which are homologous to bfeUO , respectively, AH68_00600 which is homologous to sifA (Vazquez-Gutierrez et al, 2017 ). The presence of BfeUO and SifA homologs in these three bifidobacterial strains illustrate the importance of these two iron uptake system in sequestering this vital micronutrient.…”

Section: Discussionmentioning

confidence: 99%

Genome-Wide Search for Genes Required for Bifidobacterial Growth under Iron-Limitation

et al. 2017

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Bacteria evolved over millennia in the presence of the vital micronutrient iron. Iron is involved in numerous processes within the cell and is essential for nearly all living organisms. The importance of iron to the survival of bacteria is obvious from the large variety of mechanisms by which iron may be acquired from the environment. Random mutagenesis and global gene expression profiling led to the identification of a number of genes, which are essential for Bifidobacterium breve UCC2003 survival under iron-restrictive conditions. These genes encode, among others, Fe-S cluster-associated proteins, a possible ferric iron reductase, a number of cell wall-associated proteins, and various DNA replication and repair proteins. In addition, our study identified several presumed iron uptake systems which were shown to be essential for B. breve UCC2003 growth under conditions of either ferric and/or ferrous iron chelation. Of these, two gene clusters encoding putative iron-uptake systems, bfeUO and sifABCDE, were further characterised, indicating that sifABCDE is involved in ferrous iron transport, while the bfeUO-encoded transport system imports both ferrous and ferric iron. Transcription studies showed that bfeUO and sifABCDE constitute two separate transcriptional units that are induced upon dipyridyl-mediated iron limitation. In the anaerobic gastrointestinal environment ferrous iron is presumed to be of most relevance, though a mutation in the sifABCDE cluster does not affect B. breve UCC2003's ability to colonise the gut of a murine model.

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The extracellular proteome of two Bifidobacterium species reveals different adaptation strategies to low iron conditions

Cited by 13 publications

References 81 publications

Clustering of Pan- and Core-genome of Lactobacillus provides Novel Evolutionary Insights for Differentiation

Clustering of Pan- and Core-genome of Lactobacillus provides Novel Evolutionary Insights for Differentiation

Bifidobacterium bifidum ATCC 15696 and Bifidobacterium breve 24b Metabolic Interaction Based on 2′- O -Fucosyl-Lactose Studied in Steady-State Cultures in a Freter-Style Chemostat

Genome-Wide Search for Genes Required for Bifidobacterial Growth under Iron-Limitation

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