Whole genome phylogeny of Cyanobacteria documents a distinct evolutionary trajectory of marine picocyanobacteria

During their 2.7 Gyr long evolution cyanobacteria radiated into a large number of different lineages. To better understand the evolution of cyanobacteria we compared a whole genome phylogenetic tree using 1,047 concatenated single copy orthologues of Prochlorococcus marinus MIT9313 obtained from 93 reference prokaryotic species with traditional phylogenies inferred from 16S rRNA gene and 109 genes found in all used genomes. In contrast to the traditional phylogeny, our genome wide analysis shows a split between picocyanobacteria encompassing all marine Prochlorococcus species, marine Synechococcus species, and members of freshwater Cyanobium genus (altogether referred here as the PSC clade) and the remaining groups of extant cyanobacteria. To determine the influence of the horizontal gene transfer on the overall tree topology we removed the 374 genes identified as potentially transferred genes. A newly calculated tree utilizing the remaining 673 genes displayed the same topology as the former whole genome tree with the PSC clade as a basal group of all cyanobacteria. The picocyanobacteria also exhibited distinctly larger similarity to reference bacteria's cell and genome size, carboxyzome architecture, various metabolic pathways, and chlorophyll synthesis than to the other cyanobacteria. Potentially horizontally transferred genes were found in connected chains throughout fundamental metabolic pathways suggesting that evolution of these genes was severely limited and or brought to a standstill. The environment related genes connected with metabolism of nitrogen, sulfur, and scarce seawater metals were more conserved in PSC group as they were already best tuned for its poor and stable environment. Other genes were found predominantly sequentially static as they were already accurately adapted with rare beneficial mutations. The PSC clade thus represents an isolated cyanobacterial lineage which followed a distinct evolutionary trajectory driven by its specific environment.

Community phylogenetics require phylogenies reconstructed from plastid genomes

Phylogenetic trees have been extensively used in community ecology. However, how the phylogenetic reconstruction affects ecological inferences is poorly understood. In this study, we reconstructed three different types of phylogenetic trees (a synthetic-tree generated using VPhylomaker, a barcode-tree generated using rbcL+matK+trnH-psbA and a genome-tree generated from plastid genomes) that represented an increasing level of phylogenetic resolution among 580 woody plant species from six dynamic plots in subtropical evergreen broadleaved forests of China. We then evaluated the performance of each phylogeny in estimations of community phylogenetic structure, turnover and phylogenetic signal in functional traits. As expected, the genome-tree was most resolved and most supported for relationships among species. For local phylogenetic structure, the three trees showed consistent results with Faith’s PD and MPD; however, only the synthetic-tree produced significant clustering patterns using MNTD for some plots. For phylogenetic turnover, contrasting results between the molecular trees and the synthetic-tree occurred only with nearest neighbor distance. The barcode-tree agreed more with the genome-tree than the synthetic-tree for both phylogenetic structure and turnover. For functional traits, both the barcode-tree and genome-tree detected phylogenetic signal in maximum height, but only the genome-tree detected signal in leaf width. This is the first study that uses plastid genomes in large-scale community phylogenetics. Our results highlight the outperformance of genome-trees over barcode-trees and synthetic-trees for the analyses studied here. Our results also point to the possibility of Type I and II errors in estimation of phylogenetic structure and turnover and detection of phylogenetic signal when using synthetic-trees.

Reclassification of the Taxonomic Framework of Orders Cellvibrionales, Oceanospirillales, Pseudomonadales, and Alteromonadales in Class Gammaproteobacteria through Phylogenomic Tree Analysis

The orders Cellvibrionales, Oceanospirillales, and Pseudomonadales, as three major orders of the largest bacterial class, Gammaproteobacteria, play important roles in various ecosystems as the keystone taxa of microbiomes, but their evolutionary relationship is currently polyphyletic and chaotic. Here, we constructed a bac120 tree and core-genome tree and calculated the amino acid identity (AAI) value to explore their intrinsic evolutionary history. In this study, we proposed two novel orders and three novel families. This evolution study vastly reconstructed the taxonomic framework of class Gammaproteobacteria and could provide a more distinct perspective on global distribution and evolutionary patterns of these environmental microorganisms.

Genome Tree of Life: Deep Burst of Organism Diversity

An organism Tree of Life (organism ToL) is a conceptual and metaphorical tree to capture a simplified narrative of the evolutionary course and kinship among the extant organisms of today. Such tree cannot be experimentally validated but may be reconstructed based on characteristics associated with the extant organisms. Since the whole genome sequence of an organism is, at present, the most comprehensive descriptor of the organism, a genome Tol can be an empirically derivable surrogate for the organism ToL. However, a genome ToL has been impossible to construct because of the practical reasons that experimentally determining the whole genome sequences of a large number of diverse organisms was technically impossible. Thus, for several decades, gene ToLs, based on selected genes, have been commonly used as a surrogate for the organisms ToL. This situation changed dramatically during the last several decades due to rapid advances in DNA sequencing technology. Here we describe the main features of a genome ToL that are different from those of the broadly accepted gene ToLs: (a) the first two organism groups to emerge are the founders of prokarya and eukarya, (b) they diversify into six large groups and all the founders of the groups have emerged in a “Deep Burst” at the very beginning period of the emergence of Life on Earth and (c) other differences are notable in the order of emergence of smaller groups.Significance StatementTree of Life is a conceptual and metaphorical tree that captures a simplified narrative of the evolutionary course and kinship among all living organisms of today. Since the whole genome sequence information of an organism is, at present, the most comprehensive description of the organism, we reconstructed a Genome Tree of Life using the proteome information from the whole genomes of over 4000 different living organisms on Earth. It suggests that (a) the first two primitive organism groups to emerge are the founders of prokarya and eukarya, (b) they diversify into six large groups, and (c) all the founders of the groups have emerged in a “Deep Burst” at the very beginning period of the emergence of Life on Earth.

A genome Tree of Life for the Fungi kingdom

Fungi belong to one of the largest and most diverse kingdoms of living organisms. The evolutionary kinship within a fungal population has so far been inferred mostly from the gene-information–based trees (“gene trees”), constructed commonly based on the degree of differences of proteins or DNA sequences of a small number of highly conserved genes common among the population by a multiple sequence alignment (MSA) method. Since each gene evolves under different evolutionary pressure and time scale, it has been known that one gene tree for a population may differ from other gene trees for the same population depending on the subjective selection of the genes. Within the last decade, a large number of whole-genome sequences of fungi have become publicly available, which represent, at present, the most fundamental and complete information about each fungal organism. This presents an opportunity to infer kinship among fungi using a whole-genome information-based tree (“genome tree”). The method we used allows comparison of whole-genome information without MSA, and is a variation of a computational algorithm developed to find semantic similarities or plagiarism in two books, where we represent whole-genomic information of an organism as a book of words without spaces. The genome tree reveals several significant and notable differences from the gene trees, and these differences invoke new discussions about alternative narratives for the evolution of some of the currently accepted fungal groups.

A Proposal for a Genome Similarity-Based Taxonomy for Plant-Pathogenic Bacteria that Is Sufficiently Precise to Reflect Phylogeny, Host Range, and Outbreak Affiliation Applied to Pseudomonas syringae sensu lato as a Proof of Concept

Taxonomy of plant pathogenic bacteria is challenging because pathogens of different crops often belong to the same named species but current taxonomy does not provide names for bacteria below the subspecies level. The introduction of the host range-based pathovar system in the 1980s provided a temporary solution to this problem but has many limitations. The affordability of genome sequencing now provides the opportunity for developing a new genome-based taxonomic framework. We already proposed to name individual bacterial isolates based on pairwise genome similarity. Here, we expand on this idea and propose to use genome similarity-based codes, which we now call life identification numbers (LINs), to describe and name bacterial taxa. Using 93 genomes of Pseudomonas syringae sensu lato, LINs were compared with a P. syringae genome tree whereby the assigned LINs were found to be informative of a majority of phylogenetic relationships. LINs also reflected host range and outbreak association for strains of P. syringae pathovar actinidiae, a pathovar for which many genome sequences are available. We conclude that LINs could provide the basis for a new taxonomic framework to address the shortcomings of the current pathovar system and to complement the current taxonomic system of bacteria in general.