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Using Glycolysis Enzyme Sequences to Inform Lactobacillus Phylogeny

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Using Glycolysis Enzyme Sequences to Inform Lactobacillus Phylogeny

Katelyn Brandt et al. Microb Genom.

Abstract

The genus Lactobacillus encompasses a diversity of species that occur widely in nature and encode a plethora of metabolic pathways reflecting their adaptation to various ecological niches, including humans, animals, plants and food products. Accordingly, their functional attributes have been exploited industrially and several strains are commonly formulated as probiotics or starter cultures in the food industry. Although divergent evolutionary processes have yielded the acquisition and evolution of specialized functionalities, all Lactobacillus species share a small set of core metabolic properties, including the glycolysis pathway. Thus, the sequences of glycolytic enzymes afford a means to establish phylogenetic groups with the potential to discern species that are too closely related from a 16S rRNA standpoint. Here, we identified and extracted glycolysis enzyme sequences from 52 species, and carried out individual and concatenated phylogenetic analyses. We show that a glycolysis-based phylogenetic tree can robustly segregate lactobacilli into distinct clusters and discern very closely related species. We also compare and contrast evolutionary patterns with genome-wide features and transcriptomic patterns, reflecting genomic drift trends. Overall, results suggest that glycolytic enzymes provide valuable phylogenetic insights and may constitute practical targets for evolutionary studies.

Keywords: Lactobacillus; evolution; glycolysis; phylogeny.

Conflict of interest statement

The authors declare that there are no conflicts of interest.

Figures

Fig. 1.
Fig. 1.
16S rRNA tree. Tree based on the alignment of the 16S rRNA sequences using RaxML. Bootstrap values are recorded on the nodes. Groups are coloured as follows: the L. animalis group in purple, the L. vaginalis group in green, the L. buchneri group in red, the L. rhamnosus group in yellow, the L. acidophilus group in maroon, and the L. gasseri group in blue. The representative species in each group is in bold. Species names follow the naming convention shown in Table 1.
Fig. 2.
Fig. 2.
Genomic location. Normalized glycolysis gene locations in L. acidophilus, L. amylovorus, L. crispatus, L. delbrueckii subsp. bulgaricus, L. gasseri and L. helveticus. Normalization was calculated by dividing the location on the genome by the total genome size. Right arrows indicate forward direction, left reverse direction. The genomes are organized in the 5′ to 3′ direction. Colours are as follows: pgm in red, pgi in blue, pfk in yellow, fba in dark green, tpi in purple, gap in maroon, pgk in navy, gpm in mustard, eno in light green and pyk in lavender.
Fig. 3.
Fig. 3.
Glycolysis genes transcription. Each plot represents the mRNA-Seq coverage, log2 transformed, for the corresponding glycolysis gene over its length; ±100 represents the number of bases away from the start/end of the gene. The species are plotted as follows: L. acidophilus is red, L. amylovorus in blue, L. crispatus in yellow, L. delbrueckii subsp. bulgaricus in green, L. gasseri in purple and L. helveticus in maroon.
Fig. 4.
Fig. 4.
Ranked order of mRNA expression. Top 10 % most highly expressed genes in L. acidophilus, L. amylovorus, L. crispatus, L. delbrueckii subsp. bulgaricus, L. gasseri and L. helveticus. Data is represented as a log2 transformed RPKM (Reads Per Kilobase of transcript, per Million mapped reads). Transcripts are ranked from most abundant to least abundant. Glycolysis genes are coloured as follows: pgm in red, pgi in blue, pfk in yellow, fba in dark green, tpi in purple, gap in maroon, pgk in navy, gpm in mustard, eno in light green and pyk in lavender.
Fig. 5.
Fig. 5.
Concatenated glycolysis tree. Tree based on the alignment of concatenated amino acid sequences of glycolysis enzymes using RaxML. Bootstrap values are recorded on the nodes. Groups are coloured as follows: the L. animalis group in purple, the L. vaginalis group in green, L. buchneri group in red, the L. rhamnosus group in yellow, the L. acidophilus group in maroon, and the L. gasseri group in blue. The representative species in each group is in bold. Species name follows the naming convention shown in Table 1.
Fig. 6.
Fig. 6.
G+C mol% analysis of Lactobacillus glycolysis genes. Depicted are notched boxplots of G+C mol% for each glycolysis gene, concatenated genes, 16S rRNA and total genome. Genes are placed in order of increasing median. If two notches do not overlap, it is an indication of strong evidence for differing medians.
Fig. 7.
Fig. 7.
G+C mol% analysis of Lactobacillus genomes. (a) shows the total G+C mol% for each species. Species are coloured according to their phylogenetic group. (b) shows the G+C mol% of the glycolysis genes, the concatenated glycolysis genes, the 16S rRNA and total G+C mol% for each species. Species are named according to Table 1.

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