From the <i>selfish gene</i> to <i>selfish metabolism</i>: Revisiting the central dogma

Lorenzo, Vı́ctor de

doi:10.1002/bies.201300153

Cited by 64 publications

(41 citation statements)

References 119 publications

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“…However, there are numerous circumstances in which metabolic processes causally control genetic ones (75)(76)(77), despite the fact that doing so requires a reversal of the normal explanatory order. The redox control of transcription in chloroplast-bearing cells is a clear illustration of how such a "reverse" explanation can work (77).…”

Section: Metabolic Evolutionary Explanationmentioning

confidence: 99%

Endosymbiosis and its implications for evolutionary theory

O’Malley

2015

Proc. Natl. Acad. Sci. U.S.A.

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Historically, conceptualizations of symbiosis and endosymbiosis have been pitted against Darwinian or neo-Darwinian evolutionary theory. In more recent times, Lynn Margulis has argued vigorously along these lines. However, there are only shallow grounds for finding Darwinian concepts or population genetic theory incompatible with endosymbiosis. But is population genetics sufficiently explanatory of endosymbiosis and its role in evolution? Population genetics "follows" genes, is replication-centric, and is concerned with vertically consistent genetic lineages. It may also have explanatory limitations with regard to macroevolution. Even so, asking whether population genetics explains endosymbiosis may have the question the wrong way around. We should instead be asking how explanatory of evolution endosymbiosis is, and exactly which features of evolution it might be explaining. This paper will discuss how metabolic innovations associated with endosymbioses can drive evolution and thus provide an explanatory account of important episodes in the history of life. Metabolic explanations are both proximate and ultimate, in the same way genetic explanations are. Endosymbioses, therefore, point evolutionary biology toward an important dimension of evolutionary explanation.endosymbiosis | evolutionary theory | macroevolution | eukaryogenesis | metabolism M any historical accounts have viewed organelle-producing endosymbioses and symbioses in general as competing conceptually against standard evolutionary theory. Although there are several older claims to this effect, I will focus on Lynn Margulis's conjectures about how endosymbioses can be interpreted as posing problems for neo-Darwinian evolutionary theory. My aim is to assess whether endosymbiosis does in fact put pressure on evolutionary biologists and philosophers of evolution to expand beyond gene frequencies and encompass alternative explanatory frameworks.Rather than agents of revolution bent on overthrowing evolutionary theory, it is more likely that endosymbiotic relationships offer their greatest explanatory value as model systems for macroevolution. Such systems can tell us a great deal about conflict and control dynamics in ongoing organismal interactions. They provide remarkable examples of enduring evolutionary game-changing mutualistic relationships, and call out for an account of why such relationships persist and become increasingly stable.However, instead of focusing on "informational" properties of organisms, endosymbiotic systems draw attention to metabolism as a central organizing feature of life. A metabolic perspective focuses explanatorily on biochemical networks rather than genes, on phenotypic interactions rather than informational inheritance, on communities in addition to isolated organisms and lineages, and on major diversifications in the history of life. "Endosymbiotic" views of evolution are therefore valuable for expanding evolutionary explanations, even if they do not constitute a fullblown theoretical alternative to standard evolutionary...

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Section: Metabolic Evolutionary Explanationmentioning

confidence: 99%

Endosymbiosis and its implications for evolutionary theory

O’Malley

2015

Proc. Natl. Acad. Sci. U.S.A.

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“…The classical "central dogma" of molecular biology establishes the preeminence of genes over the rest of elements in the chain of information transmission (Crick, 1958;Morange, 2008). However, an insightful discussion by de Lorenzo (2014) shows that current biochemical knowledge demands an expansion of the canonical view of the "central dogma" where metabolism takes a leading role, as the ultimate source of materials for the construction of the rest of the involved elements (DNA, RNA, proteins). In other words, the metabolome is a product of the proteome and the genome/transcriptome/proteome is a product of the metabolome (Cornish-Bowden et al, 2007).…”

Section: Discussionmentioning

confidence: 99%

“…In other words, the metabolome is a product of the proteome and the genome/transcriptome/proteome is a product of the metabolome (Cornish-Bowden et al, 2007). But de Lorenzo (2014) thinking goes further to the observation that one of the driving forces in bacterial evolution is the exploration/exploitation of new chemical landscapes. Small cells with small genomes show that this goal can be achieved by reductive evolution throughout the sharing of metabolic networks.…”

Section: Discussionmentioning

confidence: 99%

Small genomes and the difficulty to define minimal translation and metabolic machineries

Gil

Peretó

2015

Front. Ecol. Evol.

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Citation:Gil R and Peretó J (2015) Small genomes and the difficulty to define minimal translation and metabolic machineries. Front. Ecol. Evol. 3:123. doi: 10.3389/fevo.2015.00123 Small genomes and the difficulty to define minimal translation and metabolic machineries The notion of minimal life has sparked the interest of scientists in different fields, ranging from the origin-of-life research to biotechnology-oriented synthetic biology. Whether the interest is focused on the emergence of protocells out of prebiotic systems or the design of a cell chassis ready to incorporate new devices and functions, proposing minimal combinations of genes for life is not a trivial task. Using comparative genomics and biochemistry of endosymbionts (i.e., intracellular mutualistic symbionts) and intracellular parasites, we proposed a decade ago the core of a minimal gene set for a simple heterotrophic cell adapted to a chemically complex environment. In this work, we discuss the state-of-the-art of the definition of the minimal genome, based on our current knowledge about bacteria with naturally reduced genomes, including both endosymbionts and free-living cells. Any proposed minimal genome would be composed by a set of protein-coding and RNA genes involved in the flux of genetic information (from DNA to functional proteins) and a group of protein-coding sequences embodying a minimalist, stoichiometrically consistent metabolic network. Although the informational portion of the minimal genome is considered quasi-universal, previous proposals have not addressed the need of tRNA post-transcriptional modifications in order to perform their function. For this reason, we have focused on the essentiality of some enzymes involved in such modifications, in order to refine the set of informational genes. As for the metabolic aspect, an obvious difficulty is that there is no one minimal gene set for life but many, depending on the environment. Among cells with reduced genomes, we find a continuum of metabolic modes, from organic matter-dependent heterotrophy to the minimally demanding autotrophy. Both best-known cases of cells with small genomes, the endosymbionts and the ultra-small free-living bacteria, speak in favor of metabolic sharing as a strong force in genome reductive evolution. A hierarchy of minimal cells supported by different metabolic networks with a complexity inversely correlated with the chemical complexity of the environment can be postulated.

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“…We suggest taking such a metabolic viewpoint in order to obtain more functional insight into the role or similarity of the cells examined, complementary to that based on DNA sequences. This would reflect the observation that the physiology of microbes, of which metabolism is a key component, might be the key driver for their evolution (89). Regarded from this viewpoint, the Alteromonas and Pseudoalteromonas strains of Gammaproteobacteria clustered with Leeuwenhoekiella sp.…”

Section: Figmentioning

confidence: 93%

Large-Scale ¹³ C Flux Profiling Reveals Conservation of the Entner-Doudoroff Pathway as a Glycolytic Strategy among Marine Bacteria That Use Glucose

Klingner

Bartsch

Dogs

et al. 2015

Appl Environ Microbiol

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e Marine bacteria form one of the largest living surfaces on Earth, and their metabolic activity is of fundamental importance for global nutrient cycling. Here, we explored the largely unknown intracellular pathways in 25 microbes representing different classes of marine bacteria that use glucose: Alphaproteobacteria, Gammaproteobacteria, and Flavobacteriia of the Bacteriodetes phylum. We used 13 C isotope experiments to infer metabolic fluxes through their carbon core pathways. Notably, 90% of all strains studied use the Entner-Doudoroff (ED) pathway for glucose catabolism, whereas only 10% rely on the Embden-Meyerhof-Parnas (EMP) pathway. This result differed dramatically from the terrestrial model strains studied, which preferentially used the EMP pathway yielding high levels of ATP. Strains using the ED pathway exhibited a more robust resistance against the oxidative stress typically found in this environment. An important feature contributing to the preferential use of the ED pathway in the oceans could therefore be enhanced supply of NADPH through this pathway. The marine bacteria studied did not specifically rely on a distinct anaplerotic route, but the carboxylation of phosphoenolpyruvate (PEP) or pyruvate for fueling of the tricarboxylic acid (TCA) cycle was evenly distributed. The marine isolates studied belong to clades that dominate the uptake of glucose, a major carbon source for bacteria in seawater. Therefore, the ED pathway may play a significant role in the cycling of mono-and polysaccharides by bacterial communities in marine ecosystems. Marine bacteria influence global environmental dynamics in fundamental ways by controlling the biogeochemistry and productivity of the oceans (1). Due to their importance, marine microorganisms have been studied intensively (2). In particular, their mechanisms for metabolizing carbon and other nutrients have attracted attention, because they directly or indirectly affect the biogeochemical status of seawater (3). A prominent nutrient in seawater is glucose, the most abundant free neutral aldose (4). Current estimates of glucose concentrations in seawater indicate an almost ubiquitous distribution in the oceans in a nanomolar range (5). Particularly, large amounts of glucose are available in coastal habitats, e.g., during bloom situations (6). In fact, a large fraction (Ͼ30%) of bacterial growth can be supported by this monosaccharide in some oceans (7,8). Furthermore, glucose is the dominant component of dissolved polysaccharides, which constitute up to 15% of marine dissolved organic matter (9). The turnover of the (monomeric and polymeric) glucose pool in different oceanic regions ranges from days to months, and glucose assimilation in marine surface waters may represent up to 40% of bacterial carbon production (5). Taken together, bacteria that use glucose are common in the sea (10), and glucose is a representative model nutrient to monitor carbon uptake by heterotrophic marine bacteria (11). At this point, questions that arise from current knowledge concern...

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From the selfish gene to selfish metabolism: Revisiting the central dogma

Cited by 64 publications

References 119 publications

Endosymbiosis and its implications for evolutionary theory

Endosymbiosis and its implications for evolutionary theory

Small genomes and the difficulty to define minimal translation and metabolic machineries

Large-Scale ¹³ C Flux Profiling Reveals Conservation of the Entner-Doudoroff Pathway as a Glycolytic Strategy among Marine Bacteria That Use Glucose

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From the selfish gene to selfish metabolism: Revisiting the central dogma

Cited by 64 publications

References 119 publications

Endosymbiosis and its implications for evolutionary theory

Endosymbiosis and its implications for evolutionary theory

Small genomes and the difficulty to define minimal translation and metabolic machineries

Large-Scale 13 C Flux Profiling Reveals Conservation of the Entner-Doudoroff Pathway as a Glycolytic Strategy among Marine Bacteria That Use Glucose

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Large-Scale ¹³ C Flux Profiling Reveals Conservation of the Entner-Doudoroff Pathway as a Glycolytic Strategy among Marine Bacteria That Use Glucose