Some Liked It Hot: A Hypothesis Regarding Establishment of the Proto-Mitochondrial Endosymbiont During Eukaryogenesis

Cory D. Dunn

doi:10.1007/s00239-017-9809-5

Abstract

Eukaryotic cells are characterized by a considerable increase in subcellular compartmentalization when compared to prokaryotes. Most evidence suggests that the earliest eukaryotes consisted of mitochondria derived from an α-proteobacterial ancestor enclosed within an archaeal host cell. However, what benefits the archaeal host and the proto-mitochondrial endosymbiont might have obtained at the beginning of this endosymbiotic relationship remains unclear. In this work, I argue that heat generated by the proto-mitochondrion initially permitted an archaeon living at high temperatures to colonize a cooler environment, thereby removing apparent limitations on cellular complexity. Furthermore, heat generation by the endosymbiont would have provided phenotypic flexibility not available through fixed alleles selected for fitness at specific temperatures. Finally, a role for heat production by the proto-mitochondrion bridges a conceptual gap between initial endosymbiont entry to the archaeal host and a later role for mitochondrial ATP production in permitting increased cellular complexity.

Highlights

Available evidence suggests that two prokaryotes, an archaeon and a bacterium, collaborated (Margulis 1970; Stanier 1970; Schwartz and Dayhoff 1978; Doolittle 1980; McInerney et al 2014) in the eventual formation of nucleated cells with arguably (Booth and Doolittle 2015) increased complexity of form and function
It has been argued that mitochondria, and the ATP that can be generated by these compartments, permitted an expanded number of proteins, an augmented phagocytic capacity, an increase in overt specialization, and the eventual formation of complex multicellular organisms (Lane and Martin 2010; Lane 2017; Martin et al 2017)
One mechanism by which archaea appear to have adapted to reduced temperature is through abundant lateral gene transfer (LGT) from mesophilic bacteria already residing at lower temperatures (López-García et al 2015)

Summary

Introduction

Available evidence suggests that two prokaryotes, an archaeon and a bacterium, collaborated (Margulis 1970; Stanier 1970; Schwartz and Dayhoff 1978; Doolittle 1980; McInerney et al 2014) in the eventual formation of nucleated cells with arguably (Booth and Doolittle 2015) increased complexity of form and function. One mechanism by which archaea appear to have adapted to reduced temperature is through abundant lateral gene transfer (LGT) from mesophilic bacteria already residing at lower temperatures (López-García et al 2015) Such gene transfers presumably promoted improved protein folding or enzyme activity as organisms moved to colder locations. A cell might express alternative oxidases to allow greater flux of electrons through the ETC without maximal capture of energy through proton pumping, resulting in the conversion of residual energy to heat (Moore and Siedow 1991) This approach facilitates thermogenesis by some flowering plants (Wagner et al 2008) and can help maintain plant tissues at up to 35 °C above ambient temperature (Knutson 1974). One must propose that the host cell was incapable of fulfilling its ATP needs under selection and that the endosymbiont generated more ATP than it required before encountering the

A Move Toward Complexity at Lower Temperatures

Conclusion