Maximization of information transmission influences selection of native phosphorelay architectures

Rui Alves; Baldiri Salvadó; Ron Milo; Ester Vilaprinyo; Albert Sorribas

doi:10.7717/peerj.11558

Maximization of information transmission influences selection of native phosphorelay architectures

PeerJ. 2021 Jun 10:9:e11558. doi: 10.7717/peerj.11558. eCollection 2021.

Authors

Rui Alves^#¹, Baldiri Salvadó^#¹, Ron Milo², Ester Vilaprinyo¹, Albert Sorribas¹

Affiliations

¹ Ciències Mèdiques Bàsiques, Universitat de Lleida, Lleida, Spain.
² Plant and Environmental Science, Weizmann Institute of Science, Rehovot, Israel.

^# Contributed equally.

Abstract

Phosphorelays are signal transduction circuits that sense environmental changes and adjust cellular metabolism. Five different circuit architectures account for 99% of all phosphorelay operons annotated in over 9,000 fully sequenced genomes. Here we asked what biological design principles, if any, could explain selection among those architectures in nature. We began by studying kinetically well characterized phosphorelays (Spo0 of Bacillus subtilis and Sln1 of Saccharomyces cerevisiae). We find that natural circuit architecture maximizes information transmission in both cases. We use mathematical models to compare information transmission among the architectures for a realistic range of concentration and parameter values. Mapping experimentally determined phosphorelay protein concentrations onto that range reveals that the native architecture maximizes information transmission in sixteen out of seventeen analyzed phosphorelays. These results suggest that maximization of information transmission is important in the selection of native phosphorelay architectures, parameter values and protein concentrations.

Keywords: Bacterial signal transduction; Biological design principles; Biological information transmission; Mathematical modelling; Selection.

Grants and funding

The travel related to this work was funded by the Ministerio de Ciencia y educación del gobierno de España (PRX18/00142 to Rui Alves) and the publication fee was funded by the Project G20010 from Universitat de Lleida. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.