The arthrobacter arilaitensis Re117 genome sequence reveals its genetic adaptation to the surface of cheese

Abstract

Arthrobacter arilaitensis is one of the major bacterial species found at the surface of cheeses, especially in smear-ripened cheeses, where it contributes to the typical colour, flavour and texture properties of the final product. The A. arilaitensis Re117 genome is composed of a 3,859,257 bp chromosome and two plasmids of 50,407 and 8,528 bp. The chromosome shares large regions of synteny with the chromosomes of three environmental Arthrobacter strains for which genome sequences are available: A. aurescens TC1, A. chlorophenolicus A6 and Arthrobacter sp. FB24. In contrast however, 4.92% of the A. arilaitensis chromosome is composed of ISs elements, a portion that is at least 15 fold higher than for the other Arthrobacter strains. Comparative genomic analyses reveal an extensive loss of genes associated with catabolic activities, presumably as a result of adaptation to the properties of the cheese surface habitat. Like the environmental Arthrobacter strains, A. arilaitensis Re117 is well-equipped with enzymes required for the catabolism of major carbon substrates present at cheese surfaces such as fatty acids, amino acids and lactic acid. However, A. arilaitensis has several specificities which seem to be linked to its adaptation to its particular niche. These include the ability to catabolize D-galactonate, a high number of glycine betaine and related osmolyte transporters, two siderophore biosynthesis gene clusters and a high number of Fe(3+)/siderophore transport systems. In model cheese experiments, addition of small amounts of iron strongly stimulated the growth of A. arilaitensis, indicating that cheese is a highly iron-restricted medium. We suggest that there is a strong selective pressure at the surface of cheese for strains with efficient iron acquisition and salt-tolerance systems together with abilities to catabolize substrates such as lactic acid, lipids and amino acids.

Figure 1. Arthrobacter arilaitensis Re117 genome atlas.

The outermost circle (circle 1) represents the scale in Mbp. Circle 2 represents the functional category of the CDSs: green, cell envelope and related processes; blue, intermediary metabolism; yellow, information pathways; orange, other functions; dark purple, proteins of unknown function that are similar to other proteins; light purple, proteins of unknown function without similarity to other proteins. Circles 3 and 4 represent CDSs (excluding transposases) on positive (red) and negative (blue) strands. Circle 5 represents the insertion sequences (in green). Circle 6 represents rRNA (grey) and tRNA (red) genes. Circle 7 represents the pseudogenes (excluding transposase pseudogenes). Circles 8, 9 and 10 represent CDSs (in blue) orthologs (predicted as defined in section “Genome analysis and annotation”) with genes from three environmental Arthrobacter strains: A. chlorophenolicus A6 (circle 8), Arthrobacter sp. FB24 (circle 9) and A. aurescens TC1 (circle 10). Circle 11 represents genes involved in siderophore biosynthesis and export (blue) and in Fe³⁺/siderophore complexes import (red). Circle 12 and 13 represent the G+C content and GC skew (G−C)/(G+C), respectively, each plotted using a 10-kb window.

Figure 2. Genes probably involved in the catabolism of D-galactonate by A. arilaitensis Re117.

Figure 3. Catechol-type siderophore gene cluster in A. arilaitensis Re117.

Genes are coloured as categorized: non-ribosomal siderophore peptide synthetase components and accessory proteins in blue, other siderophore biosynthesis proteins in orange, MbtH-like protein in dark purple, siderophore exporter in yellow, Fe³⁺/siderophore transport components in green and siderophore-interacting protein in grey. Triangles indicate the presence of putative IdeR (iron-dependent regulator) binding sites.

Figure 4. Stimulation of growth of A. arilaitensis in model cheeses by iron.

Lactic curd was inoculated with 10⁶ cfu/g of A. arilaitensis Re117 and 10⁴ cfu/g the yeast Debaryomyces hansenii 304, without (○) or with (▵) addition of 1 mg iron per kg of curd. The values correspond to the means of three replications.