Genome selection and pangenome generation
We based our analysis on the proGenomes v.2.2 dataset containing 82,400 genomes grouped into 11,562 species (that is, specI clusters) that were defined based on 40 single-copy marker genes20. The corresponding species tree generated based on concatenated marker gene sequences was kindly provided by the authors of the proGenomes article20.
From this initial selection, we filtered out metagenome-assembled genomes, single-amplified genomes, genomes flagged as chimeric by GUNC39, genomes that were not taxonomically cohesive with the rest of the specI cluster according to GTDB26, genomes with no 16S rRNA gene sequence detected and genomes we could not confidently map to the MicrobeAtlas database (see Mapping genomes to MicrobeAtlas database OTUs below). The species tree was pruned to remove these genomes using the ETE Toolkit v.3 (ref. 40). As a result, we obtained 78,315 genomes grouped into 8,790 species. For each species, a pangenome was generated by clustering all gene sequences on 95% nucleotide sequence identity as described in ref. 41.
All gene sequences were clustered using MMseqs2 (ref. 42) with minimum overlap of 50%, minimum identity threshold of 80% and clustering mode 0. The rest of the parameters were left as default. For each gene cluster, whenever sequences originated from more than one genome within a species, we only retained sequences that were most similar to those from other species within the gene cluster. We then proceeded with gene clusters containing sequences from at least five different species. Sequences were then aligned using the automatic strategy selection option in MAFFT v.7.471 (ref. 43), with all other parameters left as default. On the basis of the multiple sequence alignment, a gene tree was generated using FastTree v.2.1.11 (ref. 44) using the generalised time-reversible model45 of nucleotide evolution, with all parameters left as default.
Before performing tree reconciliation, we subsampled the species tree using ETE Toolkit v.3 (ref. 40) to decrease computational requirements in the following manner: for each gene cluster, the species tree node corresponding to the last common ancestor of all species within the gene cluster was selected. Clades within the species tree not containing any genes from the gene cluster were collapsed for computational efficiency. Subsequently, the subsampled species tree was used to root the gene tree using the OptRoot module from RANGER-DTL v.2.0 (ref. 23). We then ran RANGER-DTL with default settings to perform gene and species tree reconciliation for a total of 500. Gene clusters in which more than 50 optimal roots were detected were not considered further. Reconciliations from each optimal root were aggregated using the AggregateRanger_recipient module from RANGER-DTL v.2.0. We used a custom script to aggregate results across optimal roots and detect tree nodes that were labelled as transfers. For downstream analysis, we considered only transfer events detected in 80% reconciliations that contained gene pairs with 0.5 minimum branch support in the gene tree. In addition, all multifurcations containing 100% identical genes from different species were considered to be transfer events.
For each genome, we counted a gene as having undergone transfer as long as its pangenome-representative gene was involved in a transfer event. For the denominator (that is, total number of genes assessed), we only considered genes if their pangenome-representative genes had passed all steps described above in HGT event detection. The number of genes transferred was then divided by the total number of genes assessed and the average based on all genomes within a species was calculated. For the examples mentioned in the main text, we used data from specI_v3_Cluster259 for A. baumannii and data from specI_v3_Cluster712 for L. monocytogenes.
The NCBI Sequence Read Archive46 was searched for samples and studies containing any of the keywords metagenomic, microb*, bacteria or archaea in their metadata. The corresponding raw sequence data (as of 7 March 2020) were downloaded and quality filtered. To assign OTU labels, quality filtered data were mapped to MAPref v.2.2.1 using MAPseq v.1.0 at a 0.5 confidence level47. We then filtered out samples containing less than 1,000 reads and/or less than 20 OTUs defined at 97% 16S rRNA gene identity and retained samples with at least 90% community coverage (calculated based on the formula in ref. 48).
NCBI Sequence Read Archive sample metadata were parsed to classify every sample into four general environments: animal, aquatic, plant and soil. Subsequently, we calculated BrayCurtis distances between all samples in the dataset and compared community compositions in samples from independent studies. When a sample was consistently similar to samples assigned to a different environment, we adjusted its environment label. In cases where samples with similar community compositions had no general agreement between assigned environments, we removed the environmental label.
We used barrnap49 with default settings to predict 16S rRNA gene sequences in the genome selection, proceeding with sequences of 50% of expected length. The sequences were then mapped to MAPref v.2.2.1 using MAPseq v.1.0 (ref. 47), retaining only sequences that mapped to an OTU with a 0.3 confidence level. Genomes containing multiple 16S rRNA gene copies were mapped to OTUs based on a majority rule (50% copies) or high confidence (at least one copy with a 0.98 confidence level). Species containing multiple genomes were mapped to OTUs based on majority (50% genomes).
For each OTU within the dataset, the average abundance was calculated separately for all samples assigned to the animal, aquatic, plant and soil environments. The OTU was then assigned to its preferred environment based on the highest of the four numbers.
Distances between gene and species pairs were extracted from the corresponding trees using the dist function in ETE Toolkit v.3 (ref. 40). To plot the distribution in Fig. 2a, only gene pairs with 0.5 minimum branch support values and 50% sequence overlap within the multiple sequence alignment were considered. Gene pairs with and without transfer events were normalized with respect to species distance by splitting the species distance distributions into 80 bins and subsampling the group with the larger number of pairs in each bin (either transfer detected or no transfer detected) to the number of pairs in the second group in the corresponding bin (either no transfer detected or transfer detected). The same procedure was performed for normalizing gene pairs with and without transfer events with respect to gene distance. After normalization, the resulting distributions were compared using the two-sided MannWhitney U-test.
To calculate gene ubiquity, we counted the number of genomes represented by a gene in each pangenome versus the total number of genomes in the species. For subsequent analysis, only species encompassing ten or more genomes were considered. We used previously defined thresholds25 to distinguish extended core genes (90% gene ubiquity) and cloud genes (15% gene ubiquity). In the species pair participating in HGT, the species with the higher gene ubiquity was labelled as the putative donor, whereas the species with the lower gene ubiquity was labelled as the putative recipient. To compare extended core and cloud genes with or without transfer events, a two-sided Fishers exact test was performed.
We used the COG category and KEGG pathway functional annotations provided by the proGenomes database after running eggNOG-mapper for eggNOG 5.0 (ref. 35). Each gene cluster was annotated to the corresponding functional categories based on the union of all gene annotations within the cluster. To analyse genes associated with the mobilome, we looked up which terms corresponded to the XMobilome: phages, transposons category in the database of COGs50,51 (mobilome, curated, in Extended Data Fig. 4). In addition, we extracted terms that contained the following keywords in the annotations provided by the proGenomes database: phage, transposon, transposase, transposition, transposable, mobile, mobilization, integrase, integration, plasmid, conjugative, conjugation, transformation and competence (mobilome, uncurated, in Extended Data Fig. 4). To analyse genes associated with transcription regulation, we extracted terms from the transcription category that contained the following keywords in the annotations provided by the proGenomes database: regulation and regulator (transcription regulation, uncurated, in Extended Data Fig. 4). We calculated a functional categorys background expectation fraction by counting the total number of genes that passed the pipeline that were annotated to this category divided by the total number of genes that passed the pipeline.
For each detected transfer event, we calculated the average species and gene distance by taking all average pairwise distances between left descendants and right descendants of the transfer event (for gene distance calculations, only gene pairs with 50% sequence overlap were considered). The resulting distribution of species and gene distances can be seen in Fig. 2e. For functional enrichment analysis, minimum and maximum species and gene distance cut-offs were selected in such a way that there were no bins without observations, with the resulting area divided into thirds. We also looked specifically at transfer events at the 0.01 and 0.05 gene distance cut-offs (approximately 99% and 95% sequence identity, respectively) as these results would be more comparable to previous studies that detected HGT events based on nearly identical sequences. We then counted the number of transfer events annotated to each functional category divided by the total number of transfer events in the area. The observed fraction of events annotated to a specific function was then tested with a two-sided binomial test against the fraction of all genes on which the pipeline was run that were annotated to this function. Resulting P values were corrected for multiple testing using the HolmSidak method.
A similar procedure was performed using KEGG ortholog annotations, grouping them into KEGG pathway maps (0910109145) for Extended Data Fig. 5 and antimicrobial resistance genes (BR:ko01504) for Extended Data Fig. 6.
We compared our functional enrichment analysis results with those from refs. 9,13,18,28,29,30,31,32,33,34. In most of these studies, functional categories were based on the COG database, with the exception of ref. 13 (with categories based on the SEED52) and refs. 9,28 (both with categories based on TIGRFAMs53). The mapping between COG categories and KEGG pathways (used in our study), SEED and TIGRFAMs can be found in Supplementary Table 1.
For our study, we considered enrichment data from the most recent transfers, that is, gene distance bins 0.000.01, 0.000.05 and 0.000.25. These three gene distance bins together with three species distance bins provided us with nine data points to consider for each functional category. We assigned a functional category to have strong evidence for enrichment or depletion in transfers if at least seven of the nine data points showed significant enrichment or depletion. We assigned a functional category to have weak evidence for enrichment or depletion in transfers if most data points showed enrichment or depletion but this was not always statistically significant.
For ref. 18, we considered the results depicted in Fig. 8d and Supplementary Table 13 of the article. We calculated the first and third quartiles of the HGT index using all genes in Supplementary Table 13. We assigned a functional category to have strong evidence for enrichment in transfers if the median HGT index from genes in this category was greater than the third quartile. We assigned a functional category to have strong evidence for depletion in transfers if the median HGT index from genes in this category was less than the first quartile. Only functional categories containing at least five genes were considered.
For ref. 34, we considered the results depicted in Fig. 9 of the article. We considered only recent HGT events (99% nucleotide sequence identity). We assigned a functional category to have strong evidence for enrichment in transfers if the median recent HGTs in this category was greater than the third quartile. We assigned a functional category to have strong evidence for depletion in transfers if the median recent HGTs in this category was less than the first quartile.
For ref. 32, we considered the results depicted in Fig. 4a (HTgenes row) of the article. We considered a functional category to have strong evidence for enrichment or depletion in transfers if the observed-to-expected ratio of orthologous groups was significantly different from one.
For ref. 31, we considered the results depicted in Supplementary Fig. 7 of the article. We considered a functional category to have strong evidence for enrichment or depletion in transfers if the relative proportion of transferred genes was significantly over- or underrepresented when compared with the set of all bacterial genes.
For ref. 30, we considered the results depicted in the first two columns of Table 3 of the article. We considered a functional category to be enriched in transfers if its relative transferability was higher than one, and to be depleted in transfers if its relative transferability was lower than one. We used a P value cut-off of 0.05 to distinguish strong and weak evidence for enrichment or depletion.
For ref. 33, we considered the results depicted in Table 2 of the article. In the table, functional categories were listed that significantly differed from the background of all gene families. We used a P value cut-off of 0.05 to distinguish strong and weak evidence for enrichment or depletion.
For ref. 29, we considered the results depicted in Fig. 4b of the article. We used Z-score cut-offs of 2 and 2 to distinguish strong and weak evidence for enrichment or depletion.
For ref. 13, we considered the results depicted in Supplementary File 6 (SEED level 1 and SEED level 2) of the article. We used a P value cut-off of 0.05 to distinguish strong and weak evidence for enrichment or depletion. We downweighted depletion evidence for the transcription (regulatory) and signal transduction categories as they both mapped to regulation and cell signalling in the SEED. For COG categories that mapped to multiple categories in the SEED, we indicated evidence based on the consensus from these categories.
For ref. 28, we considered the results depicted in Table 2 of the article. We downweighted depletion evidence for cell cycle control and mitosis and cell motility as they both mapped to the cellular processes in TIGRFAMs. We also downweighted enrichment evidence for carbohydrate transport and metabolism as there was no one-to-one mapping for this category.
For ref. 9, we considered the results depicted in Fig. 2 of the article. We considered a functional category to be enriched in transfers if the proportion of transferred genes was greater than 10%, and to be depleted in transfers if the proportion of transferred genes was less than 3%.
An OTU was detected as present in a given sample if its relative abundance was at least 0.01%. To calculate the co-occurrence between two OTUs, we counted the number of samples in which both OTUs were present and divided it by the number of samples in which the less prevalent OTU was present. Phylogenetic distances between OTUs were retrieved from the MicrobeAtlas database 16S rRNA tree using the dist function in ETE Toolkit v.3 (ref. 40).
For modelling the relationship between co-occurrence and phylogenetic distance, we only considered OTUs that exchanged at least 1 gene with 30 other OTUs and OTU pairs in which both OTUs were present in at least 20 environmental samples. The power law equation (1) is as follows:
$${{rm{CO}} approx ktimes {rm{PD}}^{a},}$$
(1)
where CO stands for co-occurrence, PD stands for phylogenetic distance, and k and a are parameters fitted using the nlstools package in R54. Model residuals were then used to calculate Spearman correlations with the number of genes transferred. To generate the background distribution, the number of genes was shuffled before calculating Spearman correlations. The resulting distributions of Spearman correlations generated based on raw co-occurrence (precorrection), model residuals (postcorrection) or background were compared with each other using the two-sided MannWhitney U-test.
The analysis depicted in Fig. 4bd has been performed using a similar set-up as described in Gene and species distance normalization. We used the 7 genes transferred cut-off to denote OTU pairs with many transfer events as this corresponded to the 80% quantile of OTU pairs with at least 1 gene transferred.
Global networks of predicted interactions were computed with FlashWeave v.0.19.0 (ref. 38). This method uses the local-to-global learning approach55 to learn the skeleton of a Bayesian network encoding putative ecological relationships between species adjusted for ecological or technical confounders. To this end, FlashWeave uses an interleaved testing scheme that (1) heuristically determines likely confounding variables for each pair of species (based on univariate associations and previous iterations of the algorithm), and (2) subsequently tests whether the focal association holds when conditioned on these candidate confounders.
The parameters used for running FlashWeave were as follows: sensitive=false, heterogeneous=true, and max_k=3 (with confounder correction) or max_k=0 (without confounder correction). With these settings, FlashWeave converts non-zero read counts to centred log-ratio-transformed values to account for compositionality and discretizes these values. Mutual information tests are then run on the discretized values. We used co-occurrence data from all 95,422 OTUs contained within the environmental sample dataset, filtering the resulting network for edges between the 4,380 OTUs for which transfer event data were generated. OTU pairs with a score higher than zero were considered as interacting. To normalize for differences in phylogenetic distance and co-occurrence distributions between species with at least seven genes transferred and species with zero or one gene transfer, the procedure described in Gene and species distance normalization was performed with simultaneous subsampling on phylogenetic distance and co-occurrence for 8080 bins.
We used the same relative abundance numbers as calculated in Preferred habitat assignment. For each OTU, we only considered its abundance within its preferred environment, denoting high-abundance OTUs as those whose abundance was above the 80% quantile in this environment. In contrast, we denoted low-abundance OTUs as those whose abundance was below the 20% quantile in this environment. OTU pairs were then sorted based on phylogenetic distance and the fraction of OTU pairs with at least one transfer event detected was calculated for each phylogenetic distance bin. Error bands were calculated using Bernoullis principle of uncertainty. Resulting fractions were then pairwise compared between the highhigh, highlow and lowlow groups using a one-sided Wilcoxon rank-sum test. Resulting P values were corrected for multiple testing using the BenjaminiHochberg method.
We computed a generalism index for each OTU reflecting its environmental flexibility. This index was calculated based on the entropy of the OTUs abundance values across the four major environments (animal, aquatic, soil and plant). OTUs with similar abundances across environments had higher entropy. OTUs with uneven abundances across environments (a higher abundance in one or a few of the environments compared with the rest) had lower entropy.
To compare inter-environmental transfers, we selected 200 OTUs assigned to each environment (see Preferred habitat assignment) that displayed the highest entropy (generalists) and 200 OTUs that displayed the lowest entropy (specialists). OTU pairs were then subsampled in such a way that phylogenetic distance distributions were equal between all environments and between generalists, specialists and all species. We then counted the fraction of OTU pairs with at least one transfer event detected. To generate the background expectation, OTU pairs from all species were subsampled to the target phylogenetic distance distribution 1,000. We then fit a normal distribution to the generated data using the fitdistr function in R56 to get an estimate of the expected mean, s.d. and range of transfer rates between different environments.
Data from Figs. 2 and 4b,c and Extended Data Figs. 16 were visualized using seaborn v.0.11.2 (ref. 57) and matplotlib v.3.5.1 (ref. 58) in Python v.3.7.4. Data from Figs. 3, 4a, and 5 and Extended Data Fig. 7 were visualized using ggplot2 v.3.3.5 (ref. 59) in R v.4.1.1.
Further information on research design is available in the Nature Portfolio Reporting Summary linked to this article.
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