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Reply

Reply to Garg and Martin: The mechanism works

View ORCID ProfileIstván Zachar, View ORCID ProfileAndrás Szilágyi, View ORCID ProfileSzabolcs Számadó, and Eörs Szathmáry
  1. aDepartment of Plant Systematics, Ecology, and Theoretical Biology, Eötvös Loránd University, Budapest 1117, Hungary;
  2. bEvolutionary Systems Research Group, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany 8237, Hungary;
  3. cCenter for the Conceptual Foundations of Science, Parmenides Foundation, 82049 Pullach/Munich, Germany;
  4. dCenter for Social Sciences, Hungarian Academy of Sciences “Lendület” Research Center for Educational and Network Studies, 1097 Budapest, Hungary

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PNAS May 15, 2018 115 (20) E4545-E4546; first published May 3, 2018; https://doi.org/10.1073/pnas.1805021115
István Zachar
aDepartment of Plant Systematics, Ecology, and Theoretical Biology, Eötvös Loránd University, Budapest 1117, Hungary;
bEvolutionary Systems Research Group, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany 8237, Hungary;
cCenter for the Conceptual Foundations of Science, Parmenides Foundation, 82049 Pullach/Munich, Germany;
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  • ORCID record for István Zachar
András Szilágyi
aDepartment of Plant Systematics, Ecology, and Theoretical Biology, Eötvös Loránd University, Budapest 1117, Hungary;
bEvolutionary Systems Research Group, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany 8237, Hungary;
cCenter for the Conceptual Foundations of Science, Parmenides Foundation, 82049 Pullach/Munich, Germany;
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  • ORCID record for András Szilágyi
Szabolcs Számadó
dCenter for Social Sciences, Hungarian Academy of Sciences “Lendület” Research Center for Educational and Network Studies, 1097 Budapest, Hungary
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  • ORCID record for Szabolcs Számadó
Eörs Szathmáry
aDepartment of Plant Systematics, Ecology, and Theoretical Biology, Eötvös Loránd University, Budapest 1117, Hungary;
bEvolutionary Systems Research Group, Centre for Ecological Research, Hungarian Academy of Sciences, Tihany 8237, Hungary;
cCenter for the Conceptual Foundations of Science, Parmenides Foundation, 82049 Pullach/Munich, Germany;
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  • For correspondence: szathmary.eors@gmail.com
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Garg and Martin (1) formulate two problems regarding our recent modeling paper (2), demonstrating how prudent predation and farming by a phagotrophic host could lead to endosymbiotic establishment and how they might have had a role in the origin of mitochondria.

We see three main problematic items in Garg and Martin’s (1) criticism. These problems concern: (i) the issue of phagotrophy without (or before) mitochondria, (ii) the question of alternative bet-hedging strategies, and (iii) the status of eukaryogenesis as an idiosyncratic megaevolutionary transition. We discuss these concerns in turn.

First, Garg and Martin (1) state that “the physiological benefit of evolving phagocytosis ... is only realized in the presence of mitochondria.” This is not so, as the free-living amitochondriate protists testify. These organisms make a living of predation without mitochondria (and hydrogenosomes or mitosomes) (3). The question of whether the evolutionary path needs an energetic boost, allegedly transiently bumping-up the genome size of the evolving lineage to up to a hundred thousand genes (4), is another matter, but this suggestion remains highly controversial (5, 6).

Second, Garg and Martin (1) point out that there are alternative strategies to hedge your bets. This is certainly true: the actual path taken is bound to be historically contingent. Certainly, there are examples in the living world that farming can work, so this idea is as good as any other. More importantly, while glycogen is synthesized by the cell at its energetic and material expense, a reproducing endosymbiont grows autonomously (there is some energetic cost to the host cell due to necessary extra nutrient transport through its membrane). As we write in our paper (2): “If the farm autonomously grows within the host, allocation becomes a neutral trait.” Nevertheless, we plan to undertake a directed modeling study of the competitive advantages of the two rival strategies involved.

Third, because of its profound uniqueness, there must have been some idiosyncratic component to eukaryogenesis. Garg and Martin (1) identify this step with the critical endosymbiotic syntrophy (cf. ref. 7); early phagocytosis with the concomitant cellular reorganization (8) is another possible, unique series of events. Martin et al. (9) present numerous arguments against early phagotrophy, but we do not consider any of them decisive; detailed elaboration of this point warrants in-depth examination. Here we just call attention to the fact that a stimulating scenario for the emergence of minimal phagocytosis (10) has escaped Garg and Martin’s (1) scrutiny.

All existing consistent scenarios for eukaryogenesis involve difficult (“improbable”), yet possible steps. The jury is out on the question of whether any of them are actual. Furthermore, the mechanism we have modeled (2) might well be a not uncommon factor behind endosymbioses.

Footnotes

  • ↵1To whom correspondence should be addressed. Email: szathmary.eors{at}gmail.com.
  • Author contributions: I.Z., A.S., S.S., and E.S. wrote the paper.

  • The authors declare no conflict of interest.

Published under the PNAS license.

References

  1. ↵
    1. Garg SG,
    2. Martin WF
    (2018) Asking endosymbionts to do an enzyme’s job. Proc Natl Acad Sci USA 115:E4543–E4544.
    OpenUrlFREE Full Text
  2. ↵
    1. Zachar I,
    2. Szilágyi A,
    3. Számadó S,
    4. Szathmáry E
    (2018) Farming the mitochondrial ancestor as a model of endosymbiotic establishment by natural selection. Proc Natl Acad Sci USA 115:E1504–E1510.
    OpenUrlAbstract/FREE Full Text
  3. ↵
    1. Cavalier-Smith T,
    2. Chao EE
    (1996) Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. J Mol Evol 43:551–562.
    OpenUrlCrossRefPubMed
  4. ↵
    1. Lane N
    (2011) Energetics and genetics across the prokaryote-eukaryote divide. Biol Direct 6:35.
    OpenUrlCrossRefPubMed
  5. ↵
    1. Zachar I,
    2. Szathmáry E
    (2017) Breath-giving cooperation: Critical review of origin of mitochondria hypotheses: Major unanswered questions point to the importance of early ecology. Biol Direct 12:19.
    OpenUrl
  6. ↵
    1. Szathmáry E
    (2015) Toward major evolutionary transitions theory 2.0. Proc Natl Acad Sci USA 112:10104–10111.
    OpenUrlAbstract/FREE Full Text
  7. ↵
    1. de Duve C
    (2007) The origin of eukaryotes: A reappraisal. Nat Rev Genet 8:395–403.
    OpenUrlCrossRefPubMed
  8. ↵
    1. Cavalier-Smith T
    (2014) The neomuran revolution and phagotrophic origin of eukaryotes and cilia in the light of intracellular coevolution and a revised tree of life. Cold Spring Harb Perspect Biol 6:a016006.
    OpenUrlAbstract/FREE Full Text
  9. ↵
    1. Martin WF,
    2. Tielens AGM,
    3. Mentel M,
    4. Garg SG,
    5. Gould SB
    (2017) The physiology of phagocytosis in the context of mitochondrial origin. Microbiol Mol Biol Rev 81:e00008–e00017.
    OpenUrl
  10. ↵
    1. Cavalier-Smith T
    (2009) Predation and eukaryote cell origins: A coevolutionary perspective. Int J Biochem Cell Biol 41:307–322.
    OpenUrlCrossRefPubMed
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Reply to Garg and Martin: The mechanism works
István Zachar, András Szilágyi, Szabolcs Számadó, Eörs Szathmáry
Proceedings of the National Academy of Sciences May 2018, 115 (20) E4545-E4546; DOI: 10.1073/pnas.1805021115

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Reply to Garg and Martin: The mechanism works
István Zachar, András Szilágyi, Szabolcs Számadó, Eörs Szathmáry
Proceedings of the National Academy of Sciences May 2018, 115 (20) E4545-E4546; DOI: 10.1073/pnas.1805021115
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