Horizontal gene transfer of a chloroplast DnaJ-Fer protein to Thaumarchaeota and the evolutionary history of the DnaK chaperone system in Archaea

ABSTRACT The arms race between bacteria and their competitors has produced an astounding variety of conflict systems that are shared via horizontal gene transfer across bacterial populations. In this issue of the Journal of Bacteriology, Burroughs and Aravind investigate how these biological conflict systems have been mixed and matched into new configurations, often with novel protein domains (A. M. Burroughs and L. Aravind, J Bacteriol 202:e00365-20, 2020, https://doi.org/10.1128/JB.00365-20). The authors additionally characterize the evolutionary history of genes in eukaryotes that appear to have been acquired from these prokaryotic defense systems.

Download Full-text

Granick revisited: Synthesizing evolutionary and ecological evidence for the late origin of bacteriochlorophyll via ghost lineages and horizontal gene transfer

PLoS ONE ◽

10.1371/journal.pone.0239248 ◽

2021 ◽

Vol 16 (1) ◽

pp. e0239248 ◽

Cited By ~ 1

Author(s):

Lewis M. Ward ◽

Patrick M. Shih

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Photosynthetic Bacteria ◽

Photosynthetic Apparatus ◽

Metagenomic Sequencing ◽

Crown Group ◽

Environmental Diversity ◽

Chlorophyll Pigments ◽

History Of

Photosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

Download Full-text

Granick Revisited: Synthesizing Evolutionary and Ecological Evidence for the Late Origin of Bacteriochlorophyll via Ghost Lineages and Horizontal Gene Transfer

10.1101/2020.09.01.277905 ◽

2020 ◽

Cited By ~ 2

Author(s):

Lewis M. Ward ◽

Patrick M. Shih

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Photosynthetic Bacteria ◽

Photosynthetic Apparatus ◽

Metagenomic Sequencing ◽

Crown Group ◽

Environmental Diversity ◽

Chlorophyll Pigments ◽

History Of

AbstractPhotosynthesis—both oxygenic and more ancient anoxygenic forms—has fueled the bulk of primary productivity on Earth since it first evolved more than 3.4 billion years ago. However, the early evolutionary history of photosynthesis has been challenging to interpret due to the sparse, scattered distribution of metabolic pathways associated with photosynthesis, long timescales of evolution, and poor sampling of the true environmental diversity of photosynthetic bacteria. Here, we reconsider longstanding hypotheses for the evolutionary history of phototrophy by leveraging recent advances in metagenomic sequencing and phylogenetics to analyze relationships among phototrophic organisms and components of their photosynthesis pathways, including reaction centers and individual proteins and complexes involved in the multi-step synthesis of (bacterio)-chlorophyll pigments. We demonstrate that components of the photosynthetic apparatus have undergone extensive, independent histories of horizontal gene transfer. This suggests an evolutionary mode by which modular components of phototrophy are exchanged between diverse taxa in a piecemeal process that has led to biochemical innovation. We hypothesize that the evolution of extant anoxygenic photosynthetic bacteria has been spurred by ecological competition and restricted niches following the evolution of oxygenic Cyanobacteria and the accumulation of O2 in the atmosphere, leading to the relatively late evolution of bacteriochlorophyll pigments and the radiation of diverse crown group anoxygenic phototrophs. This hypothesis expands on the classic “Granick hypothesis” for the stepwise evolution of biochemical pathways, synthesizing recent expansion in our understanding of the diversity of phototrophic organisms as well as their evolving ecological context through Earth history.

Download Full-text

Horizontal Gene Transfers from Bacteria toEntamoebaComplex: A Strategy for Dating Events along Species Divergence

Journal of Parasitology Research ◽

10.1155/2016/3241027 ◽

2016 ◽

Vol 2016 ◽

pp. 1-10 ◽

Cited By ~ 2

Author(s):

Miguel Romero ◽

R. Cerritos ◽

Cecilia Ximenez

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Entamoeba Histolytica ◽

Lateral Gene Transfer ◽

Adaptive Radiation ◽

Fossil Record ◽

Evolutionary History ◽

Divergence Time ◽

Eukaryotic Evolution ◽

History Of

Horizontal gene transfer has proved to be relevant in eukaryotic evolution, as it has been found more often than expected and related to adaptation to certain niches. A relatively large list of laterally transferred genes has been proposed and evaluated for the parasiteEntamoeba histolytica. The goals of this work were to elucidate the importance of lateral gene transfer along the evolutionary history of some members of the genusEntamoeba, through identifying donor groups and estimating the divergence time of some of these events. In order to estimate the divergence time of some of the horizontal gene transfer events, the dating of someEntamoebaspecies was necessary, following an indirect dating strategy based on the fossil record of plausible hosts. The divergence betweenE. histolyticaandE. nuttalliiprobably occurred 5.93 million years ago (Mya); this lineage diverged fromE. dispar9.97 Mya, while the ancestor of the latter separated fromE. invadens68.18 Mya. We estimated times for 22 transferences; the most recent occurred 31.45 Mya and the oldest 253.59 Mya. Indeed, the acquisition of genes through lateral transfer may have triggered a period of adaptive radiation, thus playing a major role in the evolution of theEntamoebagenus.

Download Full-text

Inter- and intra-domain horizontal gene transfer, gain-loss asymmetry and positive selection mark the evolutionary history of the CBM14 family

FEBS Journal ◽

10.1111/febs.13256 ◽

2015 ◽

Vol 282 (10) ◽

pp. 2014-2028 ◽

Cited By ~ 8

Author(s):

Ti-Cheng Chang ◽

Ioannis Stergiopoulos

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Positive Selection ◽

Evolutionary History ◽

History Of ◽

Gain Loss

Download Full-text

Frequent, independent transfers of a catabolic gene from bacteria to contrasted filamentous eukaryotes

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2014.0848 ◽

2014 ◽

Vol 281 (1789) ◽

pp. 20140848 ◽

Cited By ~ 27

Author(s):

Maxime Bruto ◽

Claire Prigent-Combaret ◽

Patricia Luis ◽

Yvan Moënne-Loccoz ◽

Daniel Muller

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Eukaryotic Cells ◽

Phylogenomic Analysis ◽

Catabolic Gene ◽

Bacterial Phyla ◽

Bacterial Origin ◽

History Of ◽

Complex Evolutionary History

Even genetically distant prokaryotes can exchange genes between them, and these horizontal gene transfer events play a central role in adaptation and evolution. While this was long thought to be restricted to prokaryotes, certain eukaryotes have acquired genes of bacterial origin. However, gene acquisitions in eukaryotes are thought to be much less important in magnitude than in prokaryotes. Here, we describe the complex evolutionary history of a bacterial catabolic gene that has been transferred repeatedly from different bacterial phyla to stramenopiles and fungi. Indeed, phylogenomic analysis pointed to multiple acquisitions of the gene in these filamentous eukaryotes—as many as 15 different events for 65 microeukaryotes. Furthermore, once transferred, this gene acquired introns and was found expressed in mRNA databases for most recipients. Our results show that effective inter-domain transfers and subsequent adaptation of a prokaryotic gene in eukaryotic cells can happen at an unprecedented magnitude.

Download Full-text

Horizontal gene transfer from extinct and extant lineages: biological innovation and the coral of life

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2009.0033 ◽

2009 ◽

Vol 364 (1527) ◽

pp. 2229-2239 ◽

Cited By ~ 49

Author(s):

Gregory P. Fournier ◽

Jinling Huang ◽

J. Peter Gogarten

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Evolutionary History ◽

Phylogenetic Reconstruction ◽

Gene Trees ◽

Individual Gene ◽

Evolution Of Life ◽

Domains Of Life ◽

Life On Earth ◽

Simple Tree

Horizontal gene transfer (HGT) is often considered to be a source of error in phylogenetic reconstruction, causing individual gene trees within an organismal lineage to be incongruent, obfuscating the ‘true’ evolutionary history. However, when identified as such, HGTs between divergent organismal lineages are useful, phylogenetically informative characters that can provide insight into evolutionary history. Here, we discuss several distinct HGT events involving all three domains of life, illustrating the selective advantages that can be conveyed via HGT, and the utility of HGT in aiding phylogenetic reconstruction and in dating the relative sequence of speciation events. We also discuss the role of HGT from extinct lineages, and its impact on our understanding of the evolution of life on Earth. Organismal phylogeny needs to incorporate reticulations; a simple tree does not provide an accurate depiction of the processes that have shaped life's history.

Download Full-text

Adaptation by Ancient Horizontal Acquisition of Butyrate Metabolism Genes in Aggregatibacter actinomycetemcomitans

mBio ◽

10.1128/mbio.03581-20 ◽

2021 ◽

Vol 12 (2) ◽

Author(s):

Ahmed M. Moustafa ◽

Senthil Kumar Velusamy ◽

Lidiya Denu ◽

Apurva Narechania ◽

Daniel H. Fine ◽

...

Keyword(s):

Phylogenetic Analysis ◽

Gene Transfer ◽

Horizontal Gene Transfer ◽

Strong Association ◽

Aggregatibacter Actinomycetemcomitans ◽

Short Chain ◽

Oral Microbiota ◽

Content Type ◽

History Of ◽

The Impact

ABSTRACT Like the bacterial residents of the human gut, it is likely that many of the species in the human oral microbiota have evolved to better occupy and persist in their niche. Aggregatibacter actinomycetemcomitans (Aa) is both a common colonizer of the oral cavity and has been implicated in the pathogenesis of periodontal disease. Here, we present a whole-genome phylogenetic analysis of Aa isolates from humans and nonhuman primates that revealed an ancient origin for this species and a long history of association with the Catarrhini, the lineage that includes Old World monkeys (OWM) and humans. Further genomic analysis showed a strong association with the presence of a short-chain fatty acid (SCFA) catabolism locus (atoRDAEB) in many human isolates that was absent in almost all nonhuman OWM isolates. We show that this locus was likely acquired through horizontal gene transfer. When grown under conditions that are similar to those at the subgingival site of periodontitis (anaerobic, SCFA replete), Aa strains with atoRDAEB formed robust biofilms and showed upregulation of genes involved in virulence, colonization, and immune evasion. Both an isogenic deletion mutant and nonhuman primate isolates lacking the ato locus failed to grow in a robust biofilm under these conditions, but grew well under the carbohydrate-rich conditions similar to those found above the gumline. We propose that the acquisition of the ato locus was a key evolutionary step allowing Aa to utilize SCFAs, adapt, and modulate subgingival disease. IMPORTANCE There has been considerable interest in the impact of short-chain fatty acids (SCFAs) on inflammatory effects related to the microbiome. Here, we present evidence that SCFAs may also be important in disease by providing an energy source or disease-associated cue for colonizing pathogens. We propose that SCFAs allow Aggregatibacter actinomycetemcomitans (Aa) to adapt to the subgingival anaerobic environment, which is the site of human periodontitis. Under anaerobic, SCFA-rich conditions, human-derived Aa strains that possess butyrate metabolism genes form strong biofilms and upregulate virulence genes. Our phylogenetic analysis highlights a long history of evolution of Aa with its primate hosts and suggests that the acquisition of butyrate metabolism genes may have been a critical step in allowing Aa to colonize a new niche and cause disease in humans. Overall, this study highlights the important role that horizontal gene transfer may play in microbial adaptation and the evolution of infectious disease.

Download Full-text

Thinking Twice about the Evolution of Photosynthesis

10.20944/preprints201812.0087.v2 ◽

2019 ◽

Author(s):

Tanai Cardona

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Photochemical Reaction ◽

Early History ◽

Oxygenic Photosynthesis ◽

Human Beings ◽

Cautionary Tale ◽

Anoxygenic Photosynthesis ◽

History Of ◽

Evolution Of Photosynthesis

Sam Granick opened his seminal 1957 paper titled Speculations on the Origins and Evolution of Photosynthesis with the assertion that there is a constant urge in human beings to seek beginnings (I concur). This urge has led to an incessant stream of speculative ideas and debates on the evolution of photosynthesis that started in the first half of the twentieth century and shows no signs of abating. Some of these speculative ideas have become common place, are taken as fact, but find little support. Here I review and scrutinise three widely accepted ideas that underpin the current study of the evolution of photosynthesis: firstly, that the photochemical reaction centres used in anoxygenic photosynthesis are more primitive than those in oxygenic photosynthesis; secondly, that the probability of acquiring photosynthesis via horizontal gene transfer is greater than the loss of photosynthesis; and thirdly, and most importantly, that the origin of anoxygenic photosynthesis predates the origin of oxygenic photosynthesis. I shall attempt to demonstrate that these three ideas are often grounded on incorrect assumptions built on more assumptions with no experimental nor observational support. I hope that this brief review will not only serve as cautionary tale, but also that it will open new avenues of research aimed at disentangling the complex evolution of photosynthesis and its impact on the early history of life and the planet.

Download Full-text

Repeated horizontal gene transfer of GALactose metabolism genes violates Dollo’s law of irreversible loss

10.1101/2020.07.22.216101 ◽

2020 ◽

Cited By ~ 1

Author(s):

Max A. B. Haase ◽

Jacek Kominek ◽

Dana A. Opulente ◽

Xing-Xing Shen ◽

Abigail L. LaBella ◽

...

Keyword(s):

Gene Transfer ◽

Horizontal Gene Transfer ◽

Complex Traits ◽

Galactose Metabolism ◽

History Of ◽

Dollo’S Law ◽

Ancestral States ◽

Phylogenomic Analyses ◽

Galactose Utilization ◽

Utilization Pathway

AbstractDollo’s law posits that evolutionary losses are irreversible, thereby narrowing the potential paths of evolutionary change. While phenotypic reversals to ancestral states have been observed, little is known about their underlying genetic causes. The genomes of budding yeasts have been shaped by extensive reductive evolution, such as reduced genome sizes and the losses of metabolic capabilities. However, the extent and mechanisms of trait reacquisition after gene loss in yeasts have not been thoroughly studied. Here, through phylogenomic analyses, we reconstructed the evolutionary history of the yeast galactose utilization pathway and observed widespread and repeated losses of the ability to utilize galactose, which occurred concurrently with the losses of GALactose (GAL) utilization genes. Unexpectedly, we detected three galactose-utilizing lineages that were deeply embedded within clades that underwent ancient losses of galactose utilization. We show that at least two, and possibly three, lineages reacquired the GAL pathway via yeast-to-yeast horizontal gene transfer. Our results show how trait reacquisition can occur tens of millions of years after an initial loss via horizontal gene transfer from distant relatives. These findings demonstrate that the losses of complex traits and even whole pathways are not always evolutionary dead-ends, highlighting how reversals to ancestral states can occur.

Download Full-text