tRNA functional signatures classify plastids as late-branching cyanobacteria

Lawrence, Travis J.; Amrine, Katherine C. H.; Swingley, Wesley D.; Ardell, David H.

doi:10.1186/s12862-019-1552-7

Title: tRNA functional signatures classify plastids as late-branching cyanobacteria

Abstract

Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylogenetic root of plastids remains controversial. Although a single origin of plastids by endosymbiosis is broadly supported, recent phylogenomic studies are contradictory on whether plastids branch early or late within Cyanobacteria. One underlying cause may be poor fit of evolutionary models to complex phylogenomic data. Using Posterior Predictive Analysis, we show that recently applied evolutionary models poorly fit three phylogenomic datasets curated from cyanobacteria and plastid genomes because of heterogeneities in both substitution processes across sites and of compositions across lineages. To circumvent these sources of bias, we developed CYANO-MLP, a machine learning algorithm that consistently and accurately phylogenetically classifies (“phyloclassifies”) cyanobacterial genomes to their clade of origin based on bioinformatically predicted function-informative features in tRNA gene complements. Classification of cyanobacterial genomes with CYANO-MLP is accurate and robust to deletion of clades, unbalanced sampling, and compositional heterogeneity in input tRNA data. CYANO-MLP consistently classifies plastid genomes into a late-branching cyanobacterial sub-clade containing single-cell, starch-producing, nitrogen-fixing ecotypes, consistent with metabolic and gene transfer data. Phylogenomic data of cyanobacteria and plastids exhibit both site-process heterogeneities and compositionalmore »« less

Authors:

^[1]; Amrine, Katherine C. H. ^[2]; Swingley, Wesley D. ^[3]; Ardell, David H. ^[4]

Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of California, Merced, CA (United States)
Univ. of California, Merced, CA (United States); Insight Data Science, San Francisco, CA (United States)
Northern Illinois Univ., DeKalb, IL (United States)
Univ. of California, Merced, CA (United States)

Publication Date:: 2019-12-09

Research Org.:: Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)

Sponsoring Org.:: USDOE; National Science Foundation (NSF); NIH/NIAID

OSTI Identifier:: 1606714

Grant/Contract Number:: AC05-00OR22725; INSPIRE-1344279; 1R21AI127582-0; ACI-1429783

Resource Type:: Accepted Manuscript

Journal Name:: BMC Evolutionary Biology (Online)

Additional Journal Information:: Journal Name: BMC Evolutionary Biology (Online); Journal Volume: 19; Journal Issue: 1; Journal ID: ISSN 1471-2148

Publisher:: BioMed Central

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; plastids; tRNAs; cyanobacteria; primary endosymbiosis; machine learning

Citation Formats


                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., and Ardell, David H. tRNA functional signatures classify plastids as late-branching cyanobacteria.  United States: N. p., 2019. 
Web.  doi:10.1186/s12862-019-1552-7.

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                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., & Ardell, David H. tRNA functional signatures classify plastids as late-branching cyanobacteria.  United States.  https://doi.org/10.1186/s12862-019-1552-7

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                    Lawrence, Travis J., Amrine, Katherine C. H., Swingley, Wesley D., and Ardell, David H. Mon .  
"tRNA functional signatures classify plastids as late-branching cyanobacteria".  United States.  https://doi.org/10.1186/s12862-019-1552-7.  https://www.osti.gov/servlets/purl/1606714.

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@article{osti_1606714,

  title        = {tRNA functional signatures classify plastids as late-branching cyanobacteria},

  author       = {Lawrence, Travis J. and Amrine, Katherine C. H. and Swingley, Wesley D. and Ardell, David H.},

  abstractNote = {Eukaryotes acquired the trait of oxygenic photosynthesis through endosymbiosis of the cyanobacterial progenitor of plastid organelles. Despite recent advances in the phylogenomics of Cyanobacteria, the phylogenetic root of plastids remains controversial. Although a single origin of plastids by endosymbiosis is broadly supported, recent phylogenomic studies are contradictory on whether plastids branch early or late within Cyanobacteria. One underlying cause may be poor fit of evolutionary models to complex phylogenomic data. Using Posterior Predictive Analysis, we show that recently applied evolutionary models poorly fit three phylogenomic datasets curated from cyanobacteria and plastid genomes because of heterogeneities in both substitution processes across sites and of compositions across lineages. To circumvent these sources of bias, we developed CYANO-MLP, a machine learning algorithm that consistently and accurately phylogenetically classifies (“phyloclassifies”) cyanobacterial genomes to their clade of origin based on bioinformatically predicted function-informative features in tRNA gene complements. Classification of cyanobacterial genomes with CYANO-MLP is accurate and robust to deletion of clades, unbalanced sampling, and compositional heterogeneity in input tRNA data. CYANO-MLP consistently classifies plastid genomes into a late-branching cyanobacterial sub-clade containing single-cell, starch-producing, nitrogen-fixing ecotypes, consistent with metabolic and gene transfer data. Phylogenomic data of cyanobacteria and plastids exhibit both site-process heterogeneities and compositional heterogeneities across lineages. These aspects of the data require careful modeling to avoid bias in phylogenomic estimation. Furthermore, we show that amino acid recoding strategies may be insufficient to mitigate bias from compositional heterogeneities. However, the combination of our novel tRNA-specific strategy with machine learning in CYANO-MLP appears robust to these sources of bias with high accuracy in phyloclassification of cyanobacterial genomes. CYANO-MLP consistently classifies plastids as late-branching Cyanobacteria, consistent with independent evidence from signature-based approaches and some previous phylogenetic studies.},

  doi          = {10.1186/s12862-019-1552-7},

  journal      = {BMC Evolutionary Biology (Online)},

  number       = 1,

  volume       = 19,

  place        = {United States},

  year         = {2019},

  month        = {12}

}

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MOESM1 of tRNA functional signatures classify plastids as late-branching cyanobacteria
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Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D.
figshare
DOI: 10.6084/m9.figshare.11345768
This text is a supplement to the current record

MOESM2 of tRNA functional signatures classify plastids as late-branching cyanobacteria
text, January 2019

Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D.
figshare
DOI: 10.6084/m9.figshare.11345774
This text is a supplement to the current record