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

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.

Author(s):  
Lewis M. Ward ◽  
Patrick M. Shih

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.


2020 ◽  
Vol 202 (24) ◽  
Author(s):  
Emily M. Kibby ◽  
Aaron T. Whiteley

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.


2016 ◽  
Vol 2016 ◽  
pp. 1-10 ◽  
Author(s):  
Miguel Romero ◽  
R. Cerritos ◽  
Cecilia Ximenez

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.


2012 ◽  
Vol 12 (1) ◽  
pp. 226 ◽  
Author(s):  
Céline Petitjean ◽  
David Moreira ◽  
Purificación López-García ◽  
Céline Brochier-Armanet

2020 ◽  
Author(s):  
Lewis M Ward ◽  
Usha F Lingappa ◽  
John P Grotzinger ◽  
Woodward W Fischer

Abstract Genome-resolved metagenomic sequencing approaches have led to a substantial increase in the recognized diversity of microorganisms; this included the discovery of novel metabolic pathways in previously recognized clades, and has enabled a more accurate determination of the extant distribution of key metabolisms and how they evolved over Earth history. Here, we present metagenome-assembled genomes of members of the Chloroflexota (formerly Chloroflexi or Green Nonsulfur Bacteria) order Aggregatilineales (formerly SBR1031 or Thermofonsia) discovered from sequencing of thick and expansive microbial mats present in an intertidal lagoon on Little Ambergris Cay in the Turks and Caicos Islands. These taxa included multiple new lineages of Type 2 reaction center-containing phototrophs that were not closely related to previously described phototrophic Chloroflexota—revealing a rich and intricate history of horizontal gene transfer and the evolution of phototrophy and other core metabolic pathways within this widespread phylum.


2020 ◽  
Author(s):  
Lewis M Ward ◽  
Ush Lingappa ◽  
John Grotzinger ◽  
Woodward Fischer

Abstract Genome-resolved metagenomic sequencing approaches have led to a substantial increase in the recognized diversity of microorganisms; this included the discovery of novel metabolic pathways in previously recognized clades, and has enabled a more accurate determination of the extant distribution of key metabolisms and how they evolved over Earth history. Here, we present metagenome-assembled genomes of members of the Chloroflexota (formerly Chloroflexi or Green Nonsulfur Bacteria) order Aggregatilineales (formerly SBR1031 or Thermofonsia) discovered from sequencing of thick and expansive microbial mats present in an intertidal lagoon on Little Ambergris Cay in the Turks and Caicos Islands. These taxa included multiple new lineages of Type 2 reaction center-containing phototrophs that were not closely related to previously described phototrophic Chloroflexota—revealing a rich and intricate history of horizontal gene transfer and the evolution of phototrophy and other core metabolic pathways within this widespread phylum.


2014 ◽  
Vol 281 (1789) ◽  
pp. 20140848 ◽  
Author(s):  
Maxime Bruto ◽  
Claire Prigent-Combaret ◽  
Patricia Luis ◽  
Yvan Moënne-Loccoz ◽  
Daniel Muller

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.


2016 ◽  
Vol 3 (2) ◽  
pp. 150635 ◽  
Author(s):  
Vanesa L. De Pietri ◽  
R. Paul Scofield ◽  
Nikita Zelenkov ◽  
Walter E. Boles ◽  
Trevor H. Worthy

Presbyornithids were the dominant birds in Palaeogene lacustrine assemblages, especially in the Northern Hemisphere, but are thought to have disappeared worldwide by the mid-Eocene. Now classified within Anseriformes (screamers, ducks, swans and geese), their relationships have long been obscured by their strange wader-like skeletal morphology. Reassessment of the late Oligocene South Australian material attributed to Wilaru tedfordi , long considered to be of a stone-curlew (Burhinidae, Charadriiformes), reveals that this taxon represents the first record of a presbyornithid in Australia. We also describe the larger Wilaru prideauxi sp. nov. from the early Miocene of South Australia, showing that presbyornithids survived in Australia at least until ca 22 Ma. Unlike on other continents, where presbyornithids were replaced by aquatic crown-group anatids (ducks, swans and geese), species of Wilaru lived alongside these waterfowl in Australia. The morphology of the tarsometatarsus of these species indicates that, contrary to other presbyornithids, they were predominantly terrestrial birds, which probably contributed to their long-term survival in Australia. The morphological similarity between species of Wilaru and the Eocene South American presbyornithid Telmabates antiquus supports our hypothesis of a Gondwanan radiation during the evolutionary history of the Presbyornithidae. Teviornis gobiensis from the Late Cretaceous of Mongolia is here also reassessed and confirmed as a presbyornithid. These findings underscore the temporal continuance of Australia’s vertebrates and provide a new context in which the phylogeny and evolutionary history of presbyornithids can be examined.


2009 ◽  
Vol 364 (1527) ◽  
pp. 2229-2239 ◽  
Author(s):  
Gregory P. Fournier ◽  
Jinling Huang ◽  
J. Peter Gogarten

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.


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