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

Journal Article · 09 December 2019 · BMC Evolutionary Biology (Online)

DOI: https://doi.org/10.1186/s12862-019-1552-7 · OSTI ID:1606714

^[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)

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

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

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

OSTI ID:: 1606714

Journal Information:: BMC Evolutionary Biology (Online), Vol. 19, Issue 1; ISSN 1471-2148

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

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Modeling Compositional Heterogeneity Foster, Peter G. Systematic Biology, Vol. 53, Issue 3 https://doi.org/10.1080/10635150490445779	journal	June 2004
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A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process Lartillot, Nicolas; Philippe, Hervé Molecular Biology and Evolution, Vol. 21, Issue 6 https://doi.org/10.1093/molbev/msh112	journal	June 2004
Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor Deusch, O.; Landan, G.; Roettger, M. Molecular Biology and Evolution, Vol. 25, Issue 4 https://doi.org/10.1093/molbev/msn022	journal	February 2008
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Compositional Biases among Synonymous Substitutions Cause Conflict between Gene and Protein Trees for Plastid Origins Li, Blaise; Lopes, João S.; Foster, Peter G. Molecular Biology and Evolution, Vol. 31, Issue 7 https://doi.org/10.1093/molbev/msu105	journal	May 2014
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tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence Lowe, Todd M.; Eddy, Sean R. Nucleic Acids Research, Vol. 25, Issue 5 https://doi.org/10.1093/nar/25.5.955	journal	March 1997
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Opportunities and obstacles for deep learning in biology and medicine Ching, Travers; Himmelstein, Daniel S.; Beaulieu-Jones, Brett K. Journal of The Royal Society Interface, Vol. 15, Issue 141 https://doi.org/10.1098/rsif.2017.0387	journal	April 2018
Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades Gupta, R. S. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 59, Issue 10 https://doi.org/10.1099/ijs.0.005678-0	journal	July 2009
The Phylogeny of Plastids: a Review Based on Comparisons of Small-Subunit Ribosomal rna Coding Regions Bhattacharya, Debashish; Medlin, Linda Journal of Phycology, Vol. 31, Issue 4 https://doi.org/10.1111/j.1529-8817.1995.tb02542.x	journal	August 1995
The Revised Classification of Eukaryotes Adl, Sina M.; Simpson, Alastair G. B.; Lane, Christopher E. Journal of Eukaryotic Microbiology, Vol. 59, Issue 5 https://doi.org/10.1111/j.1550-7408.2012.00644.x	journal	September 2012
tRNA Signatures Reveal a Polyphyletic Origin of SAR11 Strains among Alphaproteobacteria Amrine, Katherine C. H.; Swingley, Wesley D.; Ardell, David H. PLoS Computational Biology, Vol. 10, Issue 2 https://doi.org/10.1371/journal.pcbi.1003454	journal	February 2014

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59 BASIC BIOLOGICAL SCIENCES
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MOESM1 of tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.11345768 The current record is supplemented by this text	text	January 2019
MOESM2 of tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.11345774 The current record is supplemented by this text	text	January 2019
tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.c.4775564 The current record is supplemented by this collection	collection	January 2019
tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.c.4775564.v1 The current record is supplemented by this collection	collection	January 2019
MOESM2 of tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.11345774.v1 The current record is supplemented by this text	text	January 2019
MOESM1 of tRNA functional signatures classify plastids as late-branching cyanobacteria Lawrence, Travis J.; Amrine, Katherine CH; Swingley, Wesley D. https://doi.org/10.6084/m9.figshare.11345768.v1 The current record is supplemented by this text	text	January 2019

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

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