The genomes of polyextremophilic Cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions
- Heinrich Heine University, Germany
- Rutgers University, United States
- Arizona State University, United States
Abstract
The role and extent of horizontal gene transfer (HGT) in eukaryotes are hotly disputed topics that impact our understanding of the origin of metabolic processes and the role of organelles in cellular evolution. We addressed this issue by analyzing 10 novel Cyanidiales genomes and determined that 1% of their gene inventory is HGT-derived. Numerous HGT candidates share a close phylogenetic relationship with prokaryotes that live in similar habitats as the Cyanidiales and encode functions related to polyextremophily. HGT candidates differ from native genes in GC-content, number of splice sites, and gene expression. HGT candidates are more prone to loss, which may explain the absence of a eukaryotic pan-genome. Therefore, the lack of a pan-genome and cumulative effects fail to provide substantive arguments against our hypothesis of recurring HGT followed by differential loss in eukaryotes. The maintenance of 1% HGTs, even under selection for genome reduction, underlines the importance of non-endosymbiosis related foreign gene acquisition.
Data availability
The genomic, chloroplast and mitochondrial sequences of the 10 novel genomes, as well as gene models, ESTs, protein sequences, and gene annotations are available at http://porphyra.rutgers.edu.Raw PacBio RSII reads, and also the genomic, chloroplast and mitochondrial sequences, have been submitted to the NCBI and are retrievable via BioProject ID PRJNA512382.
-
Genome sequencing of 10 novel Cyanidiales strainsNCBI Sequence Read Archive, PRJNA512382.
-
Red Algal Resources to Promote Integrative Research in Algal GenomicsRutgers University, Red Algal.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (EXC 1028)
- Andreas P M Weber
Heinrich-Heine-Universität Düsseldorf
- Andreas P M Weber
Deutsche Forschungsgemeinschaft (WE 2231/21-1)
- Andreas P M Weber
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Paul B Rainey, Max Planck Institute for Evolutionary Biology, Germany
Version history
- Received: January 10, 2019
- Accepted: May 30, 2019
- Accepted Manuscript published: May 31, 2019 (version 1)
- Version of Record published: July 15, 2019 (version 2)
Copyright
© 2019, Rossoni et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,327
- views
-
- 497
- downloads
-
- 50
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
A two-part list of links to download the article, or parts of the article, in various formats.
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
The genomes of polyextremophilic Cyanidiales contain 1% horizontally transferred genes with diverse adaptive functions
eLife 8:e45017.
https://doi.org/10.7554/eLife.45017
Further reading
-
- Biochemistry and Chemical Biology
- Evolutionary Biology
The emergence of new protein functions is crucial for the evolution of organisms. This process has been extensively researched for soluble enzymes, but it is largely unexplored for membrane transporters, even though the ability to acquire new nutrients from a changing environment requires evolvability of transport functions. Here, we demonstrate the importance of environmental pressure in obtaining a new activity or altering a promiscuous activity in members of the amino acid-polyamine-organocation (APC)-type yeast amino acid transporters family. We identify APC members that have broader substrate spectra than previously described. Using in vivo experimental evolution, we evolve two of these transporter genes, AGP1 and PUT4, toward new substrate specificities. Single mutations on these transporters are found to be sufficient for expanding the substrate range of the proteins, while retaining the capacity to transport all original substrates. Nonetheless, each adaptive mutation comes with a distinct effect on the fitness for each of the original substrates, illustrating a trade-off between the ancestral and evolved functions. Collectively, our findings reveal how substrate-adaptive mutations in membrane transporters contribute to fitness and provide insights into how organisms can use transporter evolution to explore new ecological niches.
-
- Evolutionary Biology
- Genetics and Genomics
Copy number variation in large gene families is well characterized for plant resistance genes, but similar studies are rare in animals. The zebrafish (Danio rerio) has hundreds of NLR immune genes, making this species ideal for studying this phenomenon. By sequencing 93 zebrafish from multiple wild and laboratory populations, we identified a total of 1513 NLRs, many more than the previously known 400. Approximately half of those are present in all wild populations, but only 4% were found in 80% or more of the individual fish. Wild fish have up to two times as many NLRs per individual and up to four times as many NLRs per population than laboratory strains. In contrast to the massive variability of gene copies, nucleotide diversity in zebrafish NLR genes is very low: around half of the copies are monomorphic and the remaining ones have very few polymorphisms, likely a signature of purifying selection.
