Bacterial gene import and mesophilic adaptation in archaea

Abstract

It is widely believed that the archaeal ancestor was hyperthermophilic, but during archaeal evolution, several lineages - including haloarchaea and their sister methanogens, the Thaumarchaeota, and the uncultured Marine Group II and Marine Group III Euryarchaeota (MGII/III) - independently adapted to lower temperatures. Recent phylogenomic studies suggest that the ancestors of these lineages were recipients of massive horizontal gene transfer from bacteria. Many of the acquired genes, which are often involved in metabolism and cell envelope biogenesis, were convergently acquired by distant mesophilic archaea. In this Opinion article, we explore the intriguing hypothesis that the import of these bacterial genes was crucial for the adaptation of archaea to mesophilic lifestyles.

Figure 1. Growth temperature and horizontal gene transfer from bacteria to the archaeal lineages

a ∣ Schematic representation of a Bayesian phylogenetic tree of the Archaea domain that is rooted by bacterial sequences, based on the concatenation of 32 ribosomal proteins and 38 conserved non-ribosomal proteins (including a total of 10,963 amino acid sites). The numbers shown in the branches are posterior probabilities and maximum likelihood bootstrap values: all values at the branch points are 1/100, unless otherwise indicated. 1/- refers to boostrap values that are lower than 50, which indicates that the node is fully supported by posterior probability but unsupported by bootstrap analysis. The scale bar indicates the number of substitutions per alignment site. Median optimal growth temperatures for each of the different lineages are colour coded. For details of growth temperature values, see Supplementary information S4 (table). b ∣ The number of bona fide archaeal genes and genes imported from bacteria, for different archaeal lineages^,,. MGII/III, Marine Group II and Marine Group III euryarchaeotes; TACK, Thaumarchaeota–Aigarchaeota–Crenarchaeota– Korarchaeota.

Figure 2. Proportion of bacterial genes transferred to the ancestors of archaeal taxa as a function of average optimum growth temperature and genome size

Optimal average growth temperatures and genome sizes for the different archaeal groups are given in Supplementary information S4 (table). The numbers of genes ancestrally acquired from bacteria by various archaeal groups are those published in previous work^,,. The blue data points correspond to the proportion of horizontal gene transfer (HGT) events that are considered to be ancestral to the major archaeal taxa in REFS 29, and those that are ancestral in the Thaumarchaeota and ancestral to a lineage containing both Marine Group II and Marine Group III (MGII/III) euryarchaeotes in REF. 28. The orange data points include all of the HGT events that occurred in the major archaeal taxa as described in REFS 29, but are interpreted here to include both ancestral and recent transfers (as the approach used in these studies, may interpret some recent transfers as ancestral), together with the total number of ancestral and recent HGT events identified in the Thaumarchaeota and MGII/III euryarchaeotes in REF. 28. a ∣ The acquisition of bacterial genes is negatively correlated with average optimal growth temperature in archaea. For the blue line, R2 = 0.618 and p = 6 × 10–6 (in which R2 is the coefficient of determination and p is the p value). For the orange line, R2 = 0.552 and p = 6 × 10–6. b ∣ The acquisition of bacterial genes is positively correlated with average archaeal genome size. For the blue curve, R2 = 0.463 and p = 0.38. For the orange curve, R2 = 0.376 and p = 0.39.

Figure 3. Imported bacterial genes shared by distant lineages of mesophilic archaea

The Venn diagram shows the number of genes that have been convergently acquired by the Thaumarchaeota, a lineage containing both Marine Group II and Marine Group III (MGII/III) euryarchaeotes, and haloarchaea. The diagram is based on previously published data and includes ancient and recent gene transfers^,,; the number of genes belonging to the core (referring to ancient transfers) and shell (referring to more recent transfers) gene categories are shown in Supplementary information S1,S2 (figures).

Figure 4. Maximum likelihood phylogenetic trees showing cases of convergent bacterial gene acquisition by mesophilic archaea

a ∣ A phylogenetic tree of riboflavin synthase subunit-α; the encoding gene (ribC) was acquired independently by the ancestors of the Thaumarchaeota, a lineage containing both Marine Group II and Marine Group III (MGII/III) euryarchaeotes, and haloarchaea. The tree was reconstructed using 112 conserved amino acid positions. ribC has also been exchanged between thermophilic bacteria (Thermus spp. and Thermosipho spp.) and species in the order Thermococcales (Thermococcus spp. and Pyrococcus spp.), which shows that horizontal gene transfer (HGT) between distantly related organisms that coexist in the same habitat is possible. The two triangles for Gammaproteobacteria correspond to different species of Gammaproteobacteria that do not cluster together when using this gene as phylogenetic marker. b ∣ Phylogenetic tree of haem/copper-type cytochrome/quinol oxidase subunit 1; the encoding gene (qoxB) was acquired independently by the ancestor of MGII/III euryarchaeotes, and either the ancestor of the Thaumarchaeota or that of haloarchaea, followed by an internal archaeal transfer between the ancestors of the two latter groups. The tree was reconstructed using 439 conserved amino acid positions. Details about the phylogenetic reconstruction of each tree are provided in REF. 28 and in Supplementary information S5 (box). CFB, Cytophaga–Flavobacterium–Bacteroides (phylum Bacteroidetes).