scholarly journals Thinking twice about the evolution of photosynthesis

Open Biology ◽  
2019 ◽  
Vol 9 (3) ◽  
pp. 180246 ◽  
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 commonplace, are taken as fact, but find little support. Here, I review and scrutinize three widely accepted ideas that underpin the current study of the evolution of photosynthesis: first, that the photochemical reaction centres used in anoxygenic photosynthesis are more primitive than those in oxygenic photosynthesis; second, that the probability of acquiring photosynthesis via horizontal gene transfer is greater than the probability of losing photosynthesis; and third, and most important, that the origin of anoxygenic photosynthesis pre-dates the origin of oxygenic photosynthesis. I shall attempt to demonstrate that these three ideas are often grounded in incorrect assumptions built on more assumptions with no experimental or observational support. I hope that this brief review will not only serve as a 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.

scholarly journals Thinking Twice about the Evolution of Photosynthesis

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.

scholarly journals Thinking Twice about the Evolution of Photosynthesis

2018 ◽  
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.

scholarly journals Evolution of the 3-hydroxypropionate bicycle and recent transfer of anoxygenic photosynthesis into the Chloroflexi

2017 ◽  
Vol 114 (40) ◽  
pp. 10749-10754 ◽  
Author(s):  
Patrick M. Shih ◽  
Lewis M. Ward ◽  
Woodward W. Fischer
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Carbon Fixation ◽  
Oxygenic Photosynthesis ◽  
Geological Evidence ◽  
Anoxygenic Photosynthesis ◽  
Anoxygenic Phototrophs ◽  
Wide Range ◽  
Isotope Record ◽  
Geologic Record

Various lines of evidence from both comparative biology and the geologic record make it clear that the biochemical machinery for anoxygenic photosynthesis was present on early Earth and provided the evolutionary stock from which oxygenic photosynthesis evolved ca. 2.3 billion years ago. However, the taxonomic identity of these early anoxygenic phototrophs is uncertain, including whether or not they remain extant. Several phototrophic bacterial clades are thought to have evolved before oxygenic photosynthesis emerged, including the Chloroflexi, a phylum common across a wide range of modern environments. Although Chloroflexi have traditionally been thought to be an ancient phototrophic lineage, genomics has revealed a much greater metabolic diversity than previously appreciated. Here, using a combination of comparative genomics and molecular clock analyses, we show that phototrophic members of the Chloroflexi phylum are not particularly ancient, having evolved well after the rise of oxygen (ca. 867 million years ago), and thus cannot be progenitors of oxygenic photosynthesis. Similarly, results show that the carbon fixation pathway that defines this clade—the 3-hydroxypropionate bicycle—evolved late in Earth history as a result of a series of horizontal gene transfer events, explaining the lack of geological evidence for this pathway based on the carbon isotope record. These results demonstrate the role of horizontal gene transfer in the recent metabolic innovations expressed within this phylum, including its importance in the development of a novel carbon fixation pathway.

An Early History of Gene Transfer and Therapy

1994 ◽  
Vol 5 (4) ◽  
pp. 469-480 ◽  
Author(s):  
Jon A. Wolff ◽  
Joshua Lederberg
Keyword(s):  
Gene Transfer ◽  
Early History ◽  
History Of

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

mBio ◽  
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.

scholarly journals The Linguistics of Bacterial Conflict Systems Reveal Ancient Origins of Eukaryotic Innate Immunity

2020 ◽  
Vol 202 (24) ◽  
Author(s):  
Emily M. Kibby ◽  
Aaron T. Whiteley
Keyword(s):  
Innate Immunity ◽  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Evolutionary History ◽  
Protein Domains ◽  
Arms Race ◽  
Bacterial Populations ◽  
Defense Systems ◽  
History Of ◽  
Novel Protein

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.

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

PLoS ONE ◽  
2021 ◽  
Vol 16 (1) ◽  
pp. e0239248 ◽  
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.

scholarly journals Early Archean origin of Photosystem II

2017 ◽  
Author(s):  
Tanai Cardona ◽  
Patricia Sánchez-Baracaldo ◽  
A. William Rutherford ◽  
Anthony W. D. Larkum
Keyword(s):  
Photosystem Ii ◽  
Reaction Center ◽  
Water Oxidation ◽  
Photochemical Reaction ◽  
Early Stage ◽  
Oxygenic Photosynthesis ◽  
Recent Common Ancestor ◽  
Molecular Clocks ◽  
Most Recent Common Ancestor ◽  
History Of

AbstractPhotosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of Eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale we hypothesize that this early Archean photosystem was capable of water oxidation and had already evolved some level of protection against the formation of reactive oxygen species, which would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.

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

2020 ◽  
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.

scholarly journals Complex Evolution of Light-Dependent Protochlorophyllide Oxidoreductases in Aerobic Anoxygenic Phototrophs: Origin, Phylogeny, and Function

2020 ◽  
Author(s):  
Olga Chernomor ◽  
Lena Peters ◽  
Judith Schneidewind ◽  
Anita Loeschcke ◽  
Esther Knieps-Grünhagen ◽  
...  
Keyword(s):  
Gene Transfer ◽  
Horizontal Gene Transfer ◽  
Phylogenetic Analyses ◽  
Oxygenic Photosynthesis ◽  
Protochlorophyllide Oxidoreductase ◽  
Transfer Event ◽  
Anoxygenic Phototrophs ◽  
And Function

Abstract Light-dependent protochlorophyllide oxidoreductase (LPOR) and dark-operative protochlorophyllide oxidoreductase are evolutionary and structurally distinct enzymes that are essential for the synthesis of (bacterio)chlorophyll, the primary pigment needed for both anoxygenic and oxygenic photosynthesis. In contrast to the long-held hypothesis that LPORs are only present in oxygenic phototrophs, we recently identified a functional LPOR in the aerobic anoxygenic phototrophic bacterium (AAPB) Dinoroseobacter shibae and attributed its presence to a single horizontal gene transfer event from cyanobacteria. Here, we provide evidence for the more widespread presence of genuine LPOR enzymes in AAPBs. An exhaustive bioinformatics search identified 36 putative LPORs outside of oxygenic phototrophic bacteria (cyanobacteria) with the majority being AAPBs. Using in vitro and in vivo assays, we show that the large majority of the tested AAPB enzymes are genuine LPORs. Solution structural analyses, performed for two of the AAPB LPORs, revealed a globally conserved structure when compared with a well-characterized cyanobacterial LPOR. Phylogenetic analyses suggest that LPORs were transferred not only from cyanobacteria but also subsequently between proteobacteria and from proteobacteria to Gemmatimonadetes. Our study thus provides another interesting example for the complex evolutionary processes that govern the evolution of bacteria, involving multiple horizontal gene transfer events that likely occurred at different time points and involved different donors.

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