The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals

ABSTRACT Lynn Margulis in the 1960s elegantly proposed a shared phylogenetic history between bacteria and mitochondria; this relationship has since become a cornerstone of modern cellular biology. Yet, an interesting facet of the interaction between the microbiome and mitochondria has been mostly ig...

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Autores principales: Alfredo Franco-Obregón, Jack A. Gilbert
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:5f7138e18ce94ffdaa090f36bf63d2e12021-12-02T18:39:33ZThe Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals10.1128/mSystems.00018-172379-5077https://doaj.org/article/5f7138e18ce94ffdaa090f36bf63d2e12017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00018-17https://doaj.org/toc/2379-5077ABSTRACT Lynn Margulis in the 1960s elegantly proposed a shared phylogenetic history between bacteria and mitochondria; this relationship has since become a cornerstone of modern cellular biology. Yet, an interesting facet of the interaction between the microbiome and mitochondria has been mostly ignored, that of the systems biology relationship that underpins host health and longevity. The mitochondria are descendants of primordial aerobic pleomorphic bacteria (likely genus Rickettsia) that entered (literally and functionally) into a mutualistic partnership with ancient anaerobic microbes (likely Archaea). A stable symbiosis was established, given the metabolic versatility of the early mitochondria, which were capable of providing energy with or without oxygen, whereas nutrient gathering was the assumed responsibility of the host. While microbial relationships with single-cell protists must have occurred in the past, as they occur today, the evolution of multicellular organisms generated a new framework for symbiosis with the microbial world, taking the ancient partnership to an entirely new level. Cell-cell communication between microbes and single-cell protists was augmented through multicellularity to allow distant communication between the host cells and the microbiome, resulting in the development of complex metabolic relationships and an immune system to manage these interactions. Thus, the host is now the body and its resident mitochondria, and the microbiome is an essential supplier of metabolites that act at the level of mitochondria in skeletal muscle to stabilize host metabolism. We humans are caretakers of a profoundly vast and diverse microbiota, the majority of which resides in the gut. Indeed, the microbial genetic diversity of our microbiota outstrips our own by several orders of magnitude, and the cellular abundance is roughly equivalent to our somatic selves. Modern clinical science has elegantly highlighted the importance of the microbiome for metabolic health and well-being. This perspective underscores one fundamental facet of this symbiosis, the ancestral mitochondrion-microbiome axis.Alfredo Franco-ObregónJack A. GilbertAmerican Society for MicrobiologyarticleSCFAbutyrateellagitanninslactatemetabolicmicrobiomeMicrobiologyQR1-502ENmSystems, Vol 2, Iss 3 (2017)
institution DOAJ
collection DOAJ
language EN
topic SCFA
butyrate
ellagitannins
lactate
metabolic
microbiome
Microbiology
QR1-502
spellingShingle SCFA
butyrate
ellagitannins
lactate
metabolic
microbiome
Microbiology
QR1-502
Alfredo Franco-Obregón
Jack A. Gilbert
The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
description ABSTRACT Lynn Margulis in the 1960s elegantly proposed a shared phylogenetic history between bacteria and mitochondria; this relationship has since become a cornerstone of modern cellular biology. Yet, an interesting facet of the interaction between the microbiome and mitochondria has been mostly ignored, that of the systems biology relationship that underpins host health and longevity. The mitochondria are descendants of primordial aerobic pleomorphic bacteria (likely genus Rickettsia) that entered (literally and functionally) into a mutualistic partnership with ancient anaerobic microbes (likely Archaea). A stable symbiosis was established, given the metabolic versatility of the early mitochondria, which were capable of providing energy with or without oxygen, whereas nutrient gathering was the assumed responsibility of the host. While microbial relationships with single-cell protists must have occurred in the past, as they occur today, the evolution of multicellular organisms generated a new framework for symbiosis with the microbial world, taking the ancient partnership to an entirely new level. Cell-cell communication between microbes and single-cell protists was augmented through multicellularity to allow distant communication between the host cells and the microbiome, resulting in the development of complex metabolic relationships and an immune system to manage these interactions. Thus, the host is now the body and its resident mitochondria, and the microbiome is an essential supplier of metabolites that act at the level of mitochondria in skeletal muscle to stabilize host metabolism. We humans are caretakers of a profoundly vast and diverse microbiota, the majority of which resides in the gut. Indeed, the microbial genetic diversity of our microbiota outstrips our own by several orders of magnitude, and the cellular abundance is roughly equivalent to our somatic selves. Modern clinical science has elegantly highlighted the importance of the microbiome for metabolic health and well-being. This perspective underscores one fundamental facet of this symbiosis, the ancestral mitochondrion-microbiome axis.
format article
author Alfredo Franco-Obregón
Jack A. Gilbert
author_facet Alfredo Franco-Obregón
Jack A. Gilbert
author_sort Alfredo Franco-Obregón
title The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
title_short The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
title_full The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
title_fullStr The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
title_full_unstemmed The Microbiome-Mitochondrion Connection: Common Ancestries, Common Mechanisms, Common Goals
title_sort microbiome-mitochondrion connection: common ancestries, common mechanisms, common goals
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/5f7138e18ce94ffdaa090f36bf63d2e1
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