162:
produce biomass at a faster rate than the yeast. Producing a toxic compound, like ethanol, can slow the growth of bacteria, allowing the yeast to be more competitive. However, the yeast still had to use a portion of the sugar it consumes to produce ethanol. Crabtree-positive yeasts also have increased glycolytic flow, or increased uptake of glucose and conversion to pyruvate, which compensates for using a portion of the glucose to produce ethanol rather than biomass. Therefore, it is believed that the original driving force was to kill competitors. This is supported by research that determined the kinetic behavior of the ancestral ADH protein, which was found to be optimized to make ethanol, rather than consume it.
552:), the fermentation enzyme ADH is abundant, regardless of the oxygen level. In tobacco pollen, PDC is also highly expressed in this tissue and transcript levels are not influenced by oxygen concentration. Tobacco pollen, similar to Crabtree-positive yeast, perform high levels of fermentation dependent on the sugar supply, and not oxygen availability. In these tissues, respiration and alcoholic fermentation occur simultaneously with high sugar availability. Fermentation produces the toxic acetaldehyde and ethanol, that can build up in large quantities during pollen development. It has been hypothesized that acetaldehyde is a pollen factor that causes
375:
383:
water. During the domestication process, organisms shift from natural environments that are more variable and complex to simple and stable environments with a constant substrate. This often favors specialization adaptations in domesticated microbes, associated with relaxed selection for non-useful genes in alternative metabolic strategies or pathogenicity. Domestication might be partially responsible for the traits that promote aerobic fermentation in industrial species. Introgression and HGT is common in
593:
292:(Pdh). The kinetics of the enzymes are such that when pyruvate concentrations are high, due to a high rate of glycolysis, there is increased flux through Pdc and thus the fermentation pathway. The WGD is believed to have played a beneficial role in the evolution of the Crabtree effect in post-WGD species partially due to this increase in copy number of glycolysis genes.
112:(CNV) and differential expression in metabolic genes, and regulatory reprogramming. Research is still needed to fully understand the genomic basis of this complex phenomenon. Many Crabtree-positive yeast species are used for their fermentation ability in industrial processes in the production of wine, beer, sake, bread, and bioethanol. Through
556:. Cytoplasmic male sterility is a trait observed in maize, tobacco and other plants in which there is an inability to produce viable pollen. It is believed that this trait might be due to the expression of the fermentation genes, ADH and PDC, a lot earlier on in pollen development than normal and the accumulation of toxic aldehyde.
268:
320:. Adh1 is the major enzyme responsible for catalyzing the fermentation step from acetaldehyde to ethanol. Adh2 catalyzes the reverse reaction, consuming ethanol and converting it to acetaldehyde. The ancestral, or original, Adh had a similar function as Adh1 and after a duplication in this gene, Adh2 evolved a lower K
568:
parasites degrade glucose via aerobic fermentation. In this group, this phenomenon is not a pre-adaptation to/or remnant of anaerobic life, shown through their inability to survive in anaerobic conditions. It is believed that this phenomenon developed due to the capacity for a high glycolytic flux
497:
One of the hallmarks of cancer is altered metabolism or deregulating cellular energetics. Cancers cells often have reprogrammed their glucose metabolism to perform lactic acid fermentation, in the presence of oxygen, rather than send the pyruvate made through glycolysis to the mitochondria. This is
345:
is grown on glucose in aerobic conditions, respiration-related gene expression is repressed. Mitochondrial ribosomal proteins expression is only induced under environmental stress conditions, specifically low glucose availability. Genes involving mitochondrial energy generation and phosphorylation
258:
gene results in decreased ethanol production or fully respiratory metabolism. Thus, having an efficient glucose uptake system appears to be essential to ability of aerobic fermentation. There is a significant positive correlation between the number of hexose transporter genes and the efficiency of
161:
It is believed that a major driving force in the origin of aerobic fermentation was its simultaneous origin with modern fruit (~125 mya). These fruits provided an abundance of simple sugar food source for microbial communities, including both yeast and bacteria. Bacteria, at that time, were able to
152:
Crabtree-positive yeasts likely occurred in the interval between the ability to grow under anaerobic conditions, horizontal transfer of anaerobic DHODase (encoded by URA1 with bacteria), and the loss of respiratory chain
Complex I. A more pronounced Crabtree effect, the second step, likely occurred
588:
cytochrome oxidase mutant) strain by removing three terminal cytochrome oxidases (cydAB, cyoABCD, and cbdAB) to reduce oxygen uptake. After 60 days of adaptive evolution on glucose media, the strain displayed a mixed phenotype. In aerobic conditions, some populations' fermentation solely produced
382:
Aerobic fermentation is essential for multiple industries, resulting in human domestication of several yeast strains. Beer and other alcoholic beverages, throughout human history, have played a significant role in society through drinking rituals, providing nutrition, medicine, and uncontaminated
506:
This phenomenon is often seen as counterintuitive, since cancer cells have higher energy demands due to the continued proliferation and respiration produces significantly more ATP than glycolysis alone (fermentation produces no additional ATP). Typically, there is an up-regulation in glucose
94:, and tumor cells. Crabtree-positive yeasts will respire when grown with very low concentrations of glucose or when grown on most other carbohydrate sources. The Crabtree effect is a regulatory system whereby respiration is repressed by fermentation, except in low sugar conditions. When
283:
reaction pathway were retained in post-WGD species, significantly higher than the overall retention rate. This has been associated with an increased ability to metabolize glucose into pyruvate, or higher rate of glycolysis. After glycolysis, pyruvate can either be further broken down by
324:
for ethanol. Adh2 is believed to have increased yeast species' tolerance for ethanol and allowed
Crabtree-positive species to consume the ethanol they produced after depleting sugars. However, Adh2 and consumption of ethanol is not essential for aerobic fermentation.
507:
transporters and enzymes in the glycolysis pathway (also seen in yeast). There are many parallel aspects of aerobic fermentation in tumor cells that are also seen in
Crabtree-positive yeasts. Further research into the evolution of aerobic fermentation in yeast such as
148:(ADH) encoding genes and hexose transporters. However, recent evidence has shown that aerobic fermentation originated before the WGD and evolved as a multi-step process, potentially aided by the WGD. The origin of aerobic fermentation, or the first step, in
502:
and is associated with high consumption of glucose and a high rate of glycolysis. ATP production in these cancer cells is often only through the process of glycolysis and pyruvate is broken down by the fermentation process in the cell's cytoplasm.
165:
Further evolutionary events in the development of aerobic fermentation likely increased the efficiency of this lifestyle, including increased tolerance to ethanol and the repression of the respiratory pathway. In high sugar environments,
100:
is grown below the sugar threshold and undergoes a respiration metabolism, the fermentation pathway is still fully expressed, while the respiration pathway is only expressed relative to the sugar availability. This contrasts with the
180:
to dominate in high sugar environments evolved more recently than aerobic fermentation and is dependent on the type of high-sugar environment. Other yeasts' growth is dependent on the pH and nutrients of the high-sugar environment.
153:
near the time of the WGD event. Later evolutionary events that aided in the evolution of aerobic fermentation are better understood and outlined in the section discussing the genomic basis of the
Crabtree effect.
23:
is a metabolic process by which cells metabolize sugars via fermentation in the presence of oxygen and occurs through the repression of normal respiratory metabolism. Preference of aerobic fermentation over
1033:
Alfarouk, Khalid O.; Verduzco, Daniel; Rauch, Cyril; Muddathir, Abdel Khalig; Adil, H. H. Bashir; Elhassan, Gamal O.; Ibrahim, Muntaser E.; David Polo Orozco, Julian; Cardone, Rosa Angela (2014-01-01).
144:(WGD). A majority of Crabtree-positive yeasts are post-WGD yeasts. It was believed that the WGD was a mechanism for the development of the Crabtree effect in these species due to the duplication of
238:
lineage, and detects glucose via the cAMP-signaling pathway. The number of transporter genes vary significantly between yeast species and has continually increased during the evolution of the
346:
oxidation, which are involved in respiration, have the largest expression difference between aerobic fermentative yeast species and respiratory species. In a comparative analysis between
189:
The genomic basis of the
Crabtree effect is still being investigated, and its evolution likely involved multiple successive molecular steps that increased the efficiency of the lifestyle.
354:, both of which evolved aerobic fermentation independently, the expression pattern of these two fermentative yeasts were more similar to each other than a respiratory yeast,
1803:
Legras, Jean-Luc; Merdinoglu, Didier; Cornuet, Jean-Marie; Karst, Francis (2007-05-01). "Bread, beer and wine: Saccharomyces cerevisiae diversity reflects human history".
1161:
Baumann, Kristin; Carnicer, Marc; Dragosits, Martin; Graf, Alexandra B; Stadlmann, Johannes; Jouhten, Paula; Maaheimo, Hannu; Gasser, Brigitte; Albiol, Joan (2010-10-22).
224:
encode for glucose sensors. The number of glucose sensor genes have remained mostly consistent through the budding yeast lineage, however glucose sensors are absent from
246:
also has a high number of transporter genes compared to its close relatives. Glucose uptake is believed to be a major rate-limiting step in glycolysis and replacing
1770:
Lin, Zhenguo; Li, Wen-Hsiung (2014-01-01). "Comparative
Genomics and Evolutionary Genetics of Yeast Carbon Metabolism". In PiĆĄkur, Jure; Compagno, Concetta (eds.).
675:
PiĆĄkur, Jure; RozpÄdowska, ElĆŒbieta; Polakova, Silvia; Merico, Annamaria; Compagno, Concetta (2006-04-01). "How did
Saccharomyces evolve to become a good brewer?".
532:
to allow for glycolysis to continue. For most plant tissues, fermentation only occurs in anaerobic conditions, but there are a few exceptions. In the pollen of
1467:
Libkind, Diego; Hittinger, Chris Todd; Valério, Elisabete; Gonçalves, Carla; Dover, Jim; Johnston, Mark; Gonçalves, Paula; Sampaio, José Paulo (2011-08-30).
1036:"Glycolysis, tumor metabolism, cancer growth and dissemination. A new pH-based etiopathogenic perspective and therapeutic approach to an old cancer question"
391:
species. HGT and introgression are less common in nature than is seen during domestication pressures. For example, the important industrial yeast strain
511:
can be a useful model for understanding aerobic fermentation in tumor cells. This has a potential for better understanding cancer and cancer treatments.
569:
and the high glucose concentrations of their natural environment. The mechanism for repression of respiration in these conditions is not yet known.
108:
The evolution of aerobic fermentation likely involved multiple successive molecular steps, which included the expansion of hexose transporter genes,
2076:
Bringaud, Frédéric; RiviÚre, Loïc; Coustou, Virginie (2006-09-01). "Energy metabolism of trypanosomatids: Adaptation to available carbon sources".
1401:"The Evolution of Aerobic Fermentation in Schizosaccharomyces pombe Was Associated with Regulatory Reprogramming but not Nucleosome Reorganization"
300:
The fermentation reaction only involves two steps. Pyruvate is converted to acetaldehyde by Pdc and then acetaldehyde is converted to ethanol by
275:
After a WGD, one of the duplicated gene pair is often lost through fractionation; less than 10% of WGD gene pairs have remained in
2038:
Tadege, Million; Dupuis, Isabelle; Kuhlemeier, Cris (1999-08-01). "Ethanolic fermentation: new functions for an old pathway".
44:(ATP) in high yield, it allows proliferating cells to convert nutrients such as glucose and glutamine more efficiently into
1347:
Thomson, J Michael; Gaucher, Eric A; Burgan, Michelle F; Kee, Danny W De; Li, Tang; Aris, John P; Benner, Steven A (2005).
1104:"Yeast "Make-Accumulate-Consume" Life Strategy Evolved as a Multi-Step Process That Predates the Whole Genome Duplication"
341:
In
Crabtree-negative species, respiration related genes are highly expressed in the presence of oxygen. However, when
1787:
584:
mutant strains have been bioengineered to ferment glucose under aerobic conditions. One group developed the ECOM3 (
387:
domesticated strains. Many commercial wine strains have significant portions of their DNA derived from HGT of non-
1999:"The Warburg and Crabtree effects: On the origin of cancer cell energy metabolism and of yeast glucose repression"
378:
A close up picture of ripening wine grapes. The light white "dusting" is a film that also contains wild yeasts.
242:
lineage. Most of the transporter genes have been generated by tandem duplication, rather than from the WGD.
1219:"Expansion of Hexose Transporter Genes Was Associated with the Evolution of Aerobic Fermentation in Yeasts"
553:
462:
366:. Regulatory rewiring was likely important in the evolution of aerobic fermentation in both lineages.
975:"Aerobic Fermentation of D-Glucose by an Evolved Cytochrome Oxidase-Deficient Escherichia coli Strain"
308:
genes in
Crabtree-positive compared to Crabtree-negative species and no correlation between number of
499:
393:
226:
33:
105:, which is the inhibition of fermentation in the presence of oxygen and observed in most organisms.
474:
200:(HXT) are a group of proteins that are largely responsible for the uptake of glucose in yeast. In
141:
125:
96:
408:
This hybrid is commonly used in lager-brewing, which requires slow, low temperature fermentation.
120:, to better fit their environment. Strains evolved through mechanisms that include interspecific
403:
172:
417:
1469:"Microbe domestication and the identification of the wild genetic stock of lager-brewing yeast"
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525:
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41:
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109:
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8:
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25:
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1007:
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760:
719:
57:
2051:
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is a
Crabtree-positive yeast, which developed aerobic fermentation independently from
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2020:
1971:
1936:
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642:
1840:
950:
720:"Understanding the Warburg Effect: The Metabolic Requirements of Cell Proliferation"
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2010:
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1304:
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1184:
1174:
1163:"A multi-level study of recombinant Pichia pastoris in different oxygen conditions"
1133:
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1002:
994:
928:
870:
821:
805:
755:
739:
684:
632:
129:
121:
898:
524:
Alcoholic fermentation is often used by plants in anaerobic conditions to produce
469:, which is then converted to acetic acid. Both of these processes either generate
2122:
2015:
1998:
1611:
1128:
565:
29:
1779:
933:
916:
140:
Approximately 100 million years ago (mya), within the yeast lineage there was a
1931:
1914:
1651:"Evolution of ecological dominance of yeast species in high-sugar environments"
718:
Heiden, Matthew G. Vander; Cantley, Lewis C.; Thompson, Craig B. (2009-05-22).
267:
170:
outcompetes and dominants all other yeast species, except its closest relative
102:
53:
1872:
1558:
1285:"Increased glycolytic flux as an outcome of whole-genome duplication in yeast"
874:
688:
637:
620:
72:
Aerobic fermentation evolved independently in at least three yeast lineages (
2111:
1975:
1881:
1824:
1733:
1674:
1502:
1424:
1242:
1059:
1051:
882:
817:
751:
696:
113:
74:
1954:
Warburg, Prof Otto (1925-03-01). "ĂŒber den Stoffwechsel der Carcinomzelle".
1493:
1416:
1234:
1179:
809:
743:
2097:
2059:
2024:
1940:
1899:
1832:
1692:
1630:
1576:
1543:"The genomics of microbial domestication in the fermented food environment"
1520:
1442:
1382:
1318:
1260:
1198:
1147:
1077:
1016:
835:
792:
Dashko, Sofia; Zhou, Nerve; Compagno, Concetta; PiĆĄkur, Jure (2014-09-01).
769:
704:
596:
Myc and HIF-1 regulate glucose metabolism and stimulate the Warburg effect.
454:
271:
A scheme of transformation of glucose to alcohol by alcoholic fermentation.
1741:
942:
890:
646:
998:
442:
90:). It has also been observed in plant pollen, trypanosomatids, mutated
1967:
1300:
1102:
Hagman, Arne; SÀll, Torbjörn; Compagno, Concetta; Piskur, Jure (2013).
973:
Portnoy, Vasiliy A.; HerrgĂ„rd, Markus J.; Palsson, Bernhard Ă. (2008).
446:
280:
49:
1666:
1854:
Yating, H; Zhenzhen, X; Wolfgang, L; Hirohide, T; Fusheng, C (2022).
478:
61:
1364:
450:
430:
208:
genes have been identified and 17 encode for glucose transporters (
37:
592:
514:
1856:"Oxidative Fermentation of Acetic Acid Bacteria and Its Products"
541:
486:
470:
438:
434:
80:
45:
1466:
674:
426:
411:
1853:
1649:
Williams, Kathryn M.; Liu, Ping; Fay, Justin C. (2015-08-01).
1032:
445:, in a process called AAB oxidative fermentation (AOF). After
794:"Why, when, and how did yeast evolve alcoholic fermentation?"
533:
529:
1802:
1160:
1997:
Diaz-Ruiz, Rodrigo; Rigoulet, Michel; Devin, Anne (2011).
1349:"Resurrecting ancestral alcohol dehydrogenases from yeast"
304:(Adh). There is no significant increase in the number of
369:
1101:
856:"Aerobic fermentation during tobacco pollen development"
791:
589:
lactate, while others performed mixed-acid fermentation.
192:
1346:
184:
2075:
2037:
1996:
1708:"The molecular genetics of hexose transport in yeasts"
972:
312:
genes and efficiency of fermentation. There are five
717:
279:
genome. A little over half of WGD gene pairs in the
135:
917:"Aerobic fermentation of glucose by trypanosomatids"
329:
and other Crabtree positive species do not have the
2003:
Biochimica et Biophysica Acta (BBA) - Bioenergetics
621:"The Crabtree Effect: A Regulatory System in Yeast"
116:, these yeast species have evolved, often through
2109:
1283:Conant, Gavin C; Wolfe, Kenneth H (2007-01-01).
853:
67:
1774:. Springer Berlin Heidelberg. pp. 97â120.
1772:Molecular Mechanisms in Yeast Carbon Metabolism
1705:
1473:Proceedings of the National Academy of Sciences
515:Aerobic fermentation in other non-yeast species
465:. Ethanol is first oxidized to acetaldehyde by
1648:
1595:"Origin of the Yeast Whole-Genome Duplication"
461:, which in turn is oxidized to acetic acid by
40:. While aerobic fermentation does not produce
1547:Current Opinion in Genetics & Development
1540:
711:
412:Aerobic fermentation in acetic acid bacteria
295:
1706:Boles, E.; Hollenberg, C. P. (1997-08-01).
1399:Lin, Zhenguo; Li, Wen-Hsiung (2011-04-01).
1282:
1217:Lin, Zhenguo; Li, Wen-Hsiung (2011-01-01).
1915:"Hallmarks of Cancer: The Next Generation"
481:. This process is exploited in the use of
336:
262:
2014:
1930:
1889:
1871:
1723:
1682:
1620:
1610:
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1541:Gibbons, John G; Rinker, David C (2015).
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1308:
1250:
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1178:
1137:
1127:
1067:
1006:
932:
854:Tadege, M.; Kuhlemeier, C. (1997-10-01).
825:
759:
636:
418:Acetic acid § Oxidative fermentation
216:encodes for a galactose transporter, and
618:
591:
373:
266:
1953:
1912:
914:
333:gene and consumes ethanol very poorly.
2110:
2078:Molecular and Biochemical Parasitology
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370:Domestication and aerobic fermentation
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1216:
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1208:
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666:
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193:Expansion of hexose transporter genes
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185:Genomic basis of the Crabtree effect
2066:
1847:
1748:
1637:
1583:
1527:
1449:
1267:
132:, pseudogenization, and gene loss.
13:
1725:10.1111/j.1574-6976.1997.tb00346.x
1389:
1325:
1205:
653:
572:
564:When grown in glucose-rich media,
559:
136:Origin of Crabtree effect in yeast
14:
2139:
1913:Hanahan, Douglas (4 March 2011).
1084:
1023:
957:
905:
842:
776:
607:
156:
52:oxidation of such nutrients into
2090:10.1016/j.molbiopara.2006.03.017
1817:10.1111/j.1365-294X.2007.03266.x
473:, or shuttle electrons into the
2031:
1990:
1947:
1906:
1796:
1699:
1405:Molecular Biology and Evolution
1223:Molecular Biology and Evolution
1154:
492:
1:
2052:10.1016/S1360-1385(99)01450-8
600:
397:is an interspecies hybrid of
68:Aerobic fermentation in yeast
32:in yeast, and is part of the
2016:10.1016/j.bbabio.2010.08.010
1612:10.1371/journal.pbio.1002221
1129:10.1371/journal.pone.0068734
362:is evolutionarily closer to
254:genes with a single chimera
7:
1780:10.1007/978-3-642-55013-3_5
934:10.1096/fasebj.6.13.1397837
915:Cazzulo, Juan José (1992).
425:(AAB) incompletely oxidize
10:
2144:
1932:10.1016/j.cell.2011.02.013
1593:Wolfe, Kenneth H. (2015).
554:cytoplasmic male sterility
463:acetaldehyde dehydrogenase
415:
1873:10.3389/fmicb.2022.879246
1860:Frontiers in Microbiology
1712:FEMS Microbiology Reviews
1559:10.1016/j.gde.2015.07.003
1289:Molecular Systems Biology
689:10.1016/j.tig.2006.02.002
638:10.1099/00221287-44-2-149
550:Nicotiana plumbaginifolia
519:
394:Saccharomyces pastorianus
296:CNV in fermentation genes
227:Schizosaccharomyces pombe
1052:10.18632/oncoscience.109
979:Appl. Environ. Microbiol
619:De Deken, R. H. (1966).
475:electron transport chain
142:whole genome duplication
126:horizontal gene transfer
97:Saccharomyces cerevisiae
48:by avoiding unnecessary
2040:Trends in Plant Science
1956:Klinische Wochenschrift
1494:10.1073/pnas.1105430108
1180:10.1186/1752-0509-4-141
875:10.1023/A:1005837112653
863:Plant Molecular Biology
810:10.1111/1567-1364.12161
744:10.1126/science.1160809
337:Differential expression
263:CNV in glycolysis genes
173:Saccharomyces paradoxus
597:
459:pyruvate decarboxylase
401:and the cold tolerant
379:
290:pyruvate dehydrogenase
286:pyruvate decarboxylase
272:
42:adenosine triphosphate
28:is referred to as the
1417:10.1093/molbev/msq324
1235:10.1093/molbev/msq184
595:
467:alcohol dehydrogenase
377:
302:alcohol dehydrogenase
270:
146:alcohol dehydrogenase
110:copy number variation
999:10.1128/AEM.00880-08
483:acetic acid bacteria
423:Acetic acid bacteria
259:ethanol production.
118:artificial selection
17:Aerobic fermentation
1485:2011PNAS..10814539L
1479:(35): 14539â14544.
1167:BMC Systems Biology
1120:2013PLoSO...868734H
991:2008ApEnM..74.7561P
798:FEMS Yeast Research
736:2009Sci...324.1029V
730:(5930): 1029â1033.
498:referred to as the
198:Hexose transporters
87:Schizosaccharomyces
58:carbon-carbon bonds
26:aerobic respiration
1968:10.1007/BF01726151
1301:10.1038/msb4100170
677:Trends in Genetics
598:
453:is broken down to
380:
273:
21:aerobic glycolysis
1811:(10): 2091â2102.
1805:Molecular Ecology
1667:10.1111/evo.12707
985:(24): 7561â7569.
625:J. Gen. Microbiol
546:Nicotiana tabacum
176:. The ability of
2135:
2102:
2101:
2073:
2064:
2063:
2035:
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2018:
1994:
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1800:
1794:
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1767:
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1745:
1727:
1703:
1697:
1696:
1686:
1661:(8): 2079â2093.
1646:
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1580:
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1447:
1446:
1436:
1411:(4): 1407â1413.
1396:
1387:
1386:
1376:
1344:
1323:
1322:
1312:
1280:
1265:
1264:
1254:
1214:
1203:
1202:
1192:
1182:
1158:
1152:
1151:
1141:
1131:
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1071:
1030:
1021:
1020:
1010:
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954:
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903:
902:
860:
851:
840:
839:
829:
789:
774:
773:
763:
715:
709:
708:
672:
651:
650:
640:
616:
582:Escherichia coli
130:gene duplication
2143:
2142:
2138:
2137:
2136:
2134:
2133:
2132:
2108:
2107:
2106:
2105:
2074:
2067:
2036:
2032:
1995:
1991:
1962:(12): 534â536.
1952:
1948:
1911:
1907:
1852:
1848:
1801:
1797:
1790:
1768:
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1700:
1647:
1638:
1605:(8): e1002221.
1591:
1584:
1539:
1528:
1465:
1450:
1397:
1390:
1353:Nature Genetics
1345:
1326:
1281:
1268:
1215:
1206:
1159:
1155:
1100:
1085:
1046:(12): 777â802.
1031:
1024:
971:
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927:(13): 3153â61.
913:
906:
858:
852:
843:
790:
777:
716:
712:
673:
654:
617:
608:
603:
578:
562:
560:Trypanosomatids
528:and regenerate
522:
517:
495:
449:, the produced
420:
414:
372:
339:
323:
298:
265:
195:
187:
159:
138:
70:
30:Crabtree effect
12:
11:
5:
2141:
2131:
2130:
2125:
2120:
2104:
2103:
2065:
2046:(8): 320â325.
2030:
2009:(6): 568â576.
1989:
1946:
1925:(5): 646â674.
1905:
1846:
1795:
1788:
1747:
1698:
1636:
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1526:
1448:
1388:
1365:10.1038/ng1553
1359:(6): 630â635.
1324:
1266:
1229:(1): 131â142.
1204:
1153:
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956:
904:
869:(3): 343â354.
841:
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775:
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683:(4): 183â186.
652:
631:(2): 149â156.
605:
604:
602:
599:
577:
571:
566:trypanosomatid
561:
558:
521:
518:
516:
513:
500:Warburg effect
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413:
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371:
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264:
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194:
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186:
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158:
157:Driving forces
155:
137:
134:
103:Pasteur effect
69:
66:
60:and promoting
54:carbon dioxide
34:Warburg effect
9:
6:
4:
3:
2:
2140:
2129:
2126:
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2119:
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2022:
2017:
2012:
2008:
2004:
2000:
1993:
1985:
1981:
1977:
1973:
1969:
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1961:
1958:(in German).
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1933:
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1718:(1): 85â111.
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921:FASEB Journal
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509:S. cerevisiae
504:
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399:S. cerevisiae
396:
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389:Saccharomyces
386:
385:Saccharomyces
376:
367:
365:
361:
360:S. cerevisiae
357:
353:
352:S. cerevisiae
349:
344:
343:S. cerevisiae
334:
332:
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318:S. cerevisiae
315:
311:
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293:
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278:
277:S. cerevisiae
269:
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248:S. cerevisiae
245:
241:
240:S. cerevisiae
237:
236:Saccharomyces
233:
229:
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211:
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202:S. cerevisiae
199:
190:
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178:S. cerevisiae
175:
174:
169:
168:S. cerevisiae
163:
154:
151:
150:Saccharomyces
147:
143:
133:
131:
127:
123:
122:hybridization
119:
115:
114:domestication
111:
106:
104:
99:
98:
93:
89:
88:
83:
82:
77:
76:
75:Saccharomyces
65:
63:
59:
56:, preserving
55:
51:
47:
43:
39:
35:
31:
27:
22:
18:
2081:
2077:
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2033:
2006:
2002:
1992:
1959:
1955:
1949:
1922:
1918:
1908:
1863:
1859:
1849:
1808:
1804:
1798:
1771:
1715:
1711:
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1599:PLOS Biology
1598:
1550:
1546:
1476:
1472:
1408:
1404:
1356:
1352:
1292:
1288:
1226:
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680:
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581:
580:A couple of
579:
573:
563:
549:
545:
537:
523:
508:
505:
496:
455:acetaldehyde
421:
404:S. eubayanus
402:
398:
392:
388:
384:
381:
363:
359:
358:. However,
355:
351:
347:
342:
340:
330:
326:
317:
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309:
305:
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276:
274:
255:
251:
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188:
177:
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149:
139:
107:
95:
91:
85:
79:
73:
71:
20:
16:
15:
1040:Oncoscience
493:Tumor cells
485:to produce
443:acetic acid
364:C. albicans
356:C. albicans
38:tumor cells
2128:Metabolism
2112:Categories
2084:(1): 1â9.
1173:(1): 141.
601:References
447:glycolysis
433:, usually
416:See also:
348:Sch. pombe
327:Sch. pombe
281:glycolysis
244:Sch. pombe
232:Sch. pombe
210:HXT1-HXT17
2118:Evolution
1976:0023-2173
1882:1664-302X
1825:0962-1083
1734:0168-6445
1675:1558-5646
1655:Evolution
1503:0027-8424
1425:0737-4038
1243:0737-4038
1060:2331-4737
883:0167-4412
818:1567-1364
752:0036-8075
697:0168-9525
479:ubiquinol
316:genes in
288:(Pdc) or
62:anabolism
50:catabolic
2098:16682088
2060:10431222
2025:20804724
1941:21376230
1900:35685922
1841:13157807
1833:17498234
1693:26087012
1631:26252643
1577:26338497
1521:21873232
1443:21127171
1383:15864308
1319:17667951
1261:20660490
1199:20969759
1148:23869229
1108:PLOS ONE
1078:25621294
1017:18952873
951:35191022
836:24824836
770:19460998
705:16499989
538:Zea mays
451:pyruvate
431:alcohols
1984:2034590
1891:9171043
1742:9299703
1684:4751874
1622:4529243
1568:4695309
1553:: 1â8.
1512:3167505
1481:Bibcode
1434:3058771
1374:3618678
1310:1943425
1295:: 129.
1252:3002240
1190:2987880
1139:3711898
1116:Bibcode
1069:4303887
1008:2607145
987:Bibcode
943:1397837
891:9349258
827:4262006
761:2849637
732:Bibcode
724:Science
647:5969497
586:E. coli
576:mutants
574:E. coli
542:tobacco
487:vinegar
471:NAD(P)H
439:ethanol
435:glucose
252:HXT1-17
128:(HGT),
92:E. coli
81:Dekkera
46:biomass
2123:Yeasts
2096:
2058:
2023:
1982:
1974:
1939:
1898:
1888:
1880:
1839:
1831:
1823:
1786:
1740:
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520:Plants
427:sugars
1980:S2CID
1837:S2CID
947:S2CID
895:S2CID
859:(PDF)
534:maize
441:, to
204:, 20
2094:PMID
2056:PMID
2021:PMID
2007:1807
1972:ISSN
1937:PMID
1919:Cell
1896:PMID
1878:ISSN
1829:PMID
1821:ISSN
1784:ISBN
1738:PMID
1730:ISSN
1689:PMID
1671:ISSN
1627:PMID
1573:PMID
1517:PMID
1499:ISSN
1439:PMID
1421:ISSN
1379:PMID
1315:PMID
1257:PMID
1239:ISSN
1195:PMID
1144:PMID
1074:PMID
1056:ISSN
1013:PMID
939:PMID
887:PMID
879:ISSN
832:PMID
814:ISSN
766:PMID
748:ISSN
701:PMID
693:ISSN
643:PMID
477:via
437:and
429:and
350:and
331:ADH2
222:RGT2
220:and
218:SNF3
214:GAL2
2086:doi
2082:149
2048:doi
2011:doi
1964:doi
1927:doi
1923:144
1886:PMC
1868:doi
1813:doi
1776:doi
1720:doi
1679:PMC
1663:doi
1617:PMC
1607:doi
1563:PMC
1555:doi
1507:PMC
1489:doi
1477:108
1429:PMC
1413:doi
1369:PMC
1361:doi
1305:PMC
1297:doi
1247:PMC
1231:doi
1185:PMC
1175:doi
1134:PMC
1124:doi
1064:PMC
1048:doi
1003:PMC
995:doi
929:doi
871:doi
822:PMC
806:doi
756:PMC
740:doi
728:324
685:doi
633:doi
530:NAD
526:ATP
457:by
314:Adh
310:Pdc
306:Pdc
256:HXT
250:'s
230:.
212:),
206:HXT
36:in
19:or
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1970:.
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