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

Journal Article · · BMC Evolutionary Biology (Online)
ORCiD logo [1];  [2];  [3];  [4]
  1. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); Univ. of California, Merced, CA (United States)
  2. Univ. of California, Merced, CA (United States); Insight Data Science, San Francisco, CA (United States)
  3. Northern Illinois Univ., DeKalb, IL (United States)
  4. 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.

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 journal June 2004
Computing Bayes Factors Using Thermodynamic Integration journal April 2006
Displaying the in formation contents of structural RNA alignments: the structure logos journal January 1997
Genomes of Stigonematalean Cyanobacteria (Subsection V) and the Evolution of Oxygenic Photosynthesis from Prokaryotes to Plastids journal December 2012
The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis journal January 2011
A Bayesian Mixture Model for Across-Site Heterogeneities in the Amino-Acid Replacement Process journal June 2004
Genes of Cyanobacterial Origin in Plant Nuclear Genomes Point to a Heterocyst-Forming Plastid Ancestor journal February 2008
Metabolic Symbiosis and the Birth of the Plant Kingdom journal February 2008
Compositional Biases among Synonymous Substitutions Cause Conflict between Gene and Protein Trees for Plastid Origins journal May 2014
RNA sequence analysis using covariance models journal January 1994
Compilation of tRNA sequences and sequences of tRNA genes journal January 1996
tRNAscan-SE: A Program for Improved Detection of Transfer RNA Genes in Genomic Sequence journal March 1997
Comparative analysis of splicing of the complete set of chloroplast group II introns in three higher plant mutants journal October 1999
ARAGORN, a program to detect tRNA genes and tmRNA genes in nucleotide sequences journal January 2004
PhyloBayes MPI: Phylogenetic Reconstruction with Infinite Mixtures of Profiles in a Parallel Environment journal April 2013
Opportunities and obstacles for deep learning in biology and medicine journal April 2018
Protein signatures (molecular synapomorphies) that are distinctive characteristics of the major cyanobacterial clades journal July 2009
The Phylogeny of Plastids: a Review Based on Comparisons of Small-Subunit Ribosomal rna Coding Regions journal August 1995
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tRNA Signatures Reveal a Polyphyletic Origin of SAR11 Strains among Alphaproteobacteria journal February 2014