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Horizontal gene transfer drives the evolution of dependencies in bacteria.

ABSTRACT: Many naturally occurring bacteria lead a lifestyle of metabolic dependency for crucial resources. We do not understand what factors drive bacteria toward this lifestyle and how. Here, we systematically show the crucial role of horizontal gene transfer (HGT) in dependency evolution in bacteria. Across 835 bacterial species, we map gene gain-loss dynamics on a deep evolutionary tree and assess the impact of HGT and gene loss on metabolic networks. Our analyses suggest that HGT-enabled gene gains can affect which genes are later lost. HGT typically adds new catabolic routes to bacterial metabolic networks, leading to new metabolic interactions between bacteria. We also find that gaining new routes can promote the loss of ancestral routes ("coupled gains and losses", CGLs). Phylogenetic patterns indicate that both dependencies-mediated by CGLs and those purely by gene loss-are equally likely. Our results highlight HGT as an important driver of metabolic dependency evolution in bacteria.

SUBMITTER: Goyal A

PROVIDER: S-EPMC9108730 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Horizontal gene transfer drives the evolution of dependencies in bacteria.

Goyal Akshit A

iScience 20220427 5

Many naturally occurring bacteria lead a lifestyle of metabolic dependency for crucial resources. We do not understand what factors drive bacteria toward this lifestyle and how. Here, we systematically show the crucial role of horizontal gene transfer (HGT) in dependency evolution in bacteria. Across 835 bacterial species, we map gene gain-loss dynamics on a deep evolutionary tree and assess the impact of HGT and gene loss on metabolic networks. Our analyses suggest that HGT-enabled gene gains c ...[more]

PMID: 35586069

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Project description:BackgroundGenomes of Methanosarcina spp. are among the largest archaeal genomes. One suggested reason for that is massive horizontal gene transfer (HGT) from bacteria. Genes of bacterial origin may be involved in the central metabolism and solute transport, in particular sugar synthesis, sulfur metabolism, phosphate metabolism, DNA repair, transport of small molecules etc. Horizontally transferred (HT) genes are considered to play the key role in the ability of Methanosarcina spp. to inhabit diverse environments. At the moment, genomes of three Methanosarcina spp. have been sequenced, and while these genomes vary in length and number of protein-coding genes, they all have been shown to accumulate HT genes. However, previous estimates had been made when fewer archaeal genomes were known. Moreover, several Methanosarcinaceae genomes from other genera have been sequenced recently. Here, we revise the census of genes of bacterial origin in Methanosarcinaceae.ResultsAbout 5% of Methanosarcina genes have been shown to be horizontally transferred from various bacterial groups to the last common ancestor either of Methanosarcinaceae, or Methanosarcina, or later in the evolution. Simulation of the composition of the NCBI protein non-redundant database for different years demonstrates that the estimates of the HGT rate have decreased drastically since 2002, the year of publication of the first Methanosarcina genome. The phylogenetic distribution of HT gene donors is non-uniform. Most HT genes were transferred from Firmicutes and Proteobacteria, while no HGT events from Actinobacteria to the common ancestor of Methanosarcinaceae were found. About 50% of HT genes are involved in metabolism. Horizontal transfer of transcription factors is not common, while 46% of horizontally transferred genes have demonstrated differential expression in a variety of conditions. HGT of complete operons is relatively infrequent and half of HT genes do not belong to operons.ConclusionsWhile genes of bacterial origin are still more frequent in Methanosarcinaceae than in other Archaea, most HGT events described earlier as Methanosarcina-specific seem to have occurred before the divergence of Methanosarcinaceae. Genes horizontally transferred from bacteria to archaea neither tend to be transferred with their regulators, nor in long operons.

Dataset Information

Horizontal gene transfer drives the evolution of dependencies in bacteria.

Publications

Horizontal gene transfer drives the evolution of dependencies in bacteria.

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