Modularity and Dissipation in Evolution of Macromolecular Structures, Functions, and Networks

Caetano‐Anollés, Gustavo; Yafremava, Liudmila S.; Mittenthal, Jay E.

doi:10.1002/9780470570418.ch20

Cited by 15 publications

(24 citation statements)

References 55 publications

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“…This limitation sets the pace of proteome growth, which in the cumulative plots of Figure 2D shows domain gain always overwhelms domain loss, regardless of the superkingdom or taxonomical group of FFs that is considered. Similarly, plots of use and reuse of fold superfamilies show a clear increase in values for proteomes, starting with Archaea, then Bacteria, and finally Eukarya [48]. We reveal these same patterns if the study of FFs.…”

Section: Methodssupporting

confidence: 54%

The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms

Kim

Caetano‐Anollés

2012

BMC Evol Biol

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BackgroundThe entire evolutionary history of life can be studied using myriad sequences generated by genomic research. This includes the appearance of the first cells and of superkingdoms Archaea, Bacteria, and Eukarya. However, the use of molecular sequence information for deep phylogenetic analyses is limited by mutational saturation, differential evolutionary rates, lack of sequence site independence, and other biological and technical constraints. In contrast, protein structures are evolutionary modules that are highly conserved and diverse enough to enable deep historical exploration.ResultsHere we build phylogenies that describe the evolution of proteins and proteomes. These phylogenetic trees are derived from a genomic census of protein domains defined at the fold family (FF) level of structural classification. Phylogenomic trees of FF structures were reconstructed from genomic abundance levels of 2,397 FFs in 420 proteomes of free-living organisms. These trees defined timelines of domain appearance, with time spanning from the origin of proteins to the present. Timelines are divided into five different evolutionary phases according to patterns of sharing of FFs among superkingdoms: (1) a primordial protein world, (2) reductive evolution and the rise of Archaea, (3) the rise of Bacteria from the common ancestor of Bacteria and Eukarya and early development of the three superkingdoms, (4) the rise of Eukarya and widespread organismal diversification, and (5) eukaryal diversification. The relative ancestry of the FFs shows that reductive evolution by domain loss is dominant in the first three phases and is responsible for both the diversification of life from a universal cellular ancestor and the appearance of superkingdoms. On the other hand, domain gains are predominant in the last two phases and are responsible for organismal diversification, especially in Bacteria and Eukarya.ConclusionsThe evolution of functions that are associated with corresponding FFs along the timeline reveals that primordial metabolic domains evolved earlier than informational domains involved in translation and transcription, supporting the metabolism-first hypothesis rather than the RNA world scenario. In addition, phylogenomic trees of proteomes reconstructed from FFs appearing in each of the five phases of the protein world show that trees reconstructed from ancient domain structures were consistently rooted in archaeal lineages, supporting the proposal that the archaeal ancestor is more ancient than the ancestors of other superkingdoms.

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Section: Methodssupporting

confidence: 54%

The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms

Kim

Caetano‐Anollés

2012

BMC Evol Biol

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“…These molecular processes are responsible for the redundant appearance and accumulation of modules in the structure of living organisms [e.g., how many times particular protein domains are present in proteomes (i.e., genomic abundance)] [24]. The structural hierarchy defined in the Structural Classification of Proteins (SCOP) groups protein domains with high sequence conservation (>30% identities) into fold families (FFs), FFs with structural and functional evidence of common origin into fold superfamilies (FSFs), FSFs with common topologies (i.e., same major secondary structure in same arrangement) into folds (Fs) and Fs with similar secondary structure (e.g., alpha helix, beta sheet etc.)…”

Section: Introductionmentioning

confidence: 99%

“…Because domains defined at higher levels of SCOP classification (i.e., FSFs) exhibit higher levels of evolutionary conservation than domains defined at the lower fold family (FF) or sequence levels, they make useful tools (phylogenetic characters) when studying the evolution of protein domains and organisms [28,29]. This focus on structure as general evolutionary principle of biology offers several advantages over standard phylogenetic methods and overcomes important limitations imposed by the violation of assumptions that occur when attempting to extract deep phylogenetic signal present in molecular sequence data [24]. For example, phylogenomic trees derived from genomic abundance counts of FF and FSF domains [28,30] are less prone to the effects of HGT as shown in a number of studies [29,31-34] and do not require computation of sequence alignment, making them free from the problems resulting from characters that are not applicable to data sets (i.e., insertion/deletions in sequence alignment) [35,36].…”

Section: Introductionmentioning

confidence: 99%

Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya

2012

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BackgroundThe discovery of giant viruses with genome and physical size comparable to cellular organisms, remnants of protein translation machinery and virus-specific parasites (virophages) have raised intriguing questions about their origin. Evidence advocates for their inclusion into global phylogenomic studies and their consideration as a distinct and ancient form of life.ResultsHere we reconstruct phylogenies describing the evolution of proteomes and protein domain structures of cellular organisms and double-stranded DNA viruses with medium-to-very-large proteomes (giant viruses). Trees of proteomes define viruses as a ‘fourth supergroup’ along with superkingdoms Archaea, Bacteria, and Eukarya. Trees of domains indicate they have evolved via massive and primordial reductive evolutionary processes. The distribution of domain structures suggests giant viruses harbor a significant number of protein domains including those with no cellular representation. The genomic and structural diversity embedded in the viral proteomes is comparable to the cellular proteomes of organisms with parasitic lifestyles. Since viral domains are widespread among cellular species, we propose that viruses mediate gene transfer between cells and crucially enhance biodiversity.ConclusionsResults call for a change in the way viruses are perceived. They likely represent a distinct form of life that either predated or coexisted with the last universal common ancestor (LUCA) and constitute a very crucial part of our planet’s biosphere.

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“…What drives their generation? We have made the case that information dissipation and modularity pervade biological structure in a way that maximizes energy and information flux through a system 61 . We used Layzer's far-fromequilibrium cosmological model to argue that a simple conservation law links information and entropy.…”

Section: Discussionmentioning

confidence: 99%

Evolution of Macromolecular Structure: A ‘Double Tale’ of Biological Accretion and Diversification

Caetano-Anollés

Caetano‐Anollés

2018

Science Progress

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The evolution of structure in biology is driven by accretion and change. Accretion brings together disparate parts to form bigger wholes. Change provides opportunities for growth and innovation. Here we review patterns and processes that are responsible for a 'double tale' of evolutionary accretion at various levels of complexity, from proteins and nucleic acids to high-rise building structures in cities. Parts are at first weakly linked and associate variously. As they diversify, they compete with each other and are selected for performance. The emerging interactions constrain their structure and associations. This causes parts to self-organize into modules with tight linkage. In a second phase, variants of the modules evolve and become new parts for a new generative cycle of higher-level organization. Evolutionary genomics and network biology support the 'double tale' of structural module creation and validate an evolutionary principle of maximum abundance that drives the gain and loss of modules.

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Modularity and Dissipation in Evolution of Macromolecular Structures, Functions, and Networks

Cited by 15 publications

References 55 publications

The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms

The evolutionary history of protein fold families and proteomes confirms that the archaeal ancestor is more ancient than the ancestors of other superkingdoms

Giant viruses coexisted with the cellular ancestors and represent a distinct supergroup along with superkingdoms Archaea, Bacteria and Eukarya

Evolution of Macromolecular Structure: A ‘Double Tale’ of Biological Accretion and Diversification

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