Nutrition or nature: using elementary flux modes to disentangle the complex forces shaping prokaryote pan-genomes

Daniel R Garza, F A Bastiaan von Meijenfeldt, Bram van Dijk, Annemarie Boleij, Martijn A Huynen, Bas E Dutilh

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

BACKGROUND: Microbial pan-genomes are shaped by a complex combination of stochastic and deterministic forces. Even closely related genomes exhibit extensive variation in their gene content. Understanding what drives this variation requires exploring the interactions of gene products with each other and with the organism's external environment. However, to date, conceptual models of pan-genome dynamics often represent genes as independent units and provide limited information about their mechanistic interactions.

RESULTS: We simulated the stochastic process of gene-loss using the pooled genome-scale metabolic reaction networks of 46 taxonomically diverse bacterial and archaeal families as proxies for their pan-genomes. The frequency by which reactions are retained in functional networks when stochastic gene loss is simulated in diverse environments allowed us to disentangle the metabolic reactions whose presence depends on the metabolite composition of the external environment (constrained by "nutrition") from those that are independent of the environment (constrained by "nature"). By comparing the frequency of reactions from the first group with their observed frequencies in bacterial and archaeal families, we predicted the metabolic niches that shaped the genomic composition of these lineages. Moreover, we found that the lineages that were shaped by a more diverse metabolic niche also occur in more diverse biomes as assessed by global environmental sequencing datasets.

CONCLUSION: We introduce a computational framework for analyzing and interpreting pan-reactomes that provides novel insights into the ecological and evolutionary drivers of pan-genome dynamics.

Original languageEnglish
Article number101
Pages (from-to)1-16
Number of pages16
JournalBMC ecology and evolution
Volume22
Issue number1
DOIs
Publication statusPublished - Dec 2022

Bibliographical note

Funding Information:
DRG was supported by CNPq Science Without Borders. FABvM and BED were supported by the Netherlands Organization for Scientific Research (NWO) Vidi grant 864.14.004 and European Research Council (ERC) Consolidator grant 865694: DiversiPHI. BED was supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Germany’s Excellence Strategy – EXC 2051 – Project-ID 390713860.

Publisher Copyright:
© 2022, The Author(s).

Keywords

  • Gene frequency distribution
  • Genome-scale metabolic models
  • Pan-genome evolution
  • Prokaryote evolution
  • Reactomes

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