Annual Review of Earth and Planetary Sciences Toward a Natural History of Microbial Life

Annual Review of Earth and Planetary Sciences Toward a Natural History of Microbial Life

Abstract

For most of Earth's history life was microbial, with archaeal and bacterial cells mediating biogeochemical cycles through their metabolisms and ecologies. This diversity was sufficient to maintain a habitable planet across dramatic environmental transitions during the Archean and Proterozoic Eons. However, our knowledge of the first three billion years of the biosphere pales in comparison to the rich narrative of complex life documented through the Phanerozoic geological record. In this review, we attempt to lay out a microbial natural history framework that highlights recent and ongoing research unifying microbiology, geochemistry, and traditional organismal evolutionary biology, and we propose six broadly applicable principles to aid in these endeavors. In this way, the evolutionary history of microbial life-once considered only a prelude to the much more storied history of complex metazoan life in the Phanerozoic-is finally coming into its own.

The outlines of microbial natural history are now starting to appear through the integration of genomic and geological records.

Microorganisms drive Earth's biogeochemical cycles, and their natural history reflects a coevolution with the planet.

Past environmental changes have induced microbial biotic transitions, marked by extinction, taxonomic shifts, and new metabolisms and ecologies.

Microbial evolution can benefit from a historical perspective of processes and successions as established by macropaleontology.

One. INTRODUCTION

For over two centuries, it has been recognized that the diversity of fossil forms preserved in the geological record reveals that life on Earth has changed over time, constituting a natural history. However, until very recently microorganisms have been largely absent from this account. Although they were discovered in the late sixteen hundreds, it would be another two hundred years before bacteria were firmly established as living things akin to macroscopic organisms, surreptitiously around the same time as Darwin's work establishing evolutionary adaptation through natural selection, in which they were largely omitted. Even today, the otherness of single-celled organisms-devoid of tissues, anatomical development, and clear sets of inherited morphological characters, but often easy to grow in culture and manipulate experimentally-has subjected them to entirely different kinds of scientific inquiry than what evolutionary biology has traditionally relied upon. While some early attempts were made to establish a natural history of microorganisms using physiological and morphological characteristics, in the absence of modern molecular methods, these efforts had limited power, for reasons further discussed in Section Two.

In more recent decades, the development of genomics and molecular phylogenetics raised the possibility of reconstructing a comprehensive natural history of life on Earth that includes microbial diversity and evolution. It is now understood that there is a universality of genetic inheritance that provides evolutionary continuity between microbial and complex multicellular life. Sequence-based phylogenetic reconstructions of the relationships between different groups of microorganisms also firmly establish the existence of microbial organismal lineages, analogous to those within more complex life. Additionally, the phylogeny of individual gene families can now be reconstructed, tracing the history of microbial metabolic processes that are biogeochemically significant in planetary history. Molecular phylogenetics thereby not only reveals the record of microbial lineages and metabolisms preserved within genomes but also empowers other scientific tools for reconstructing a more comprehensive natural history of the Earth-life system. Phylogenetics also enables many additional powerful methodologies, including estimating divergence times of genes and lineages using molecular clocks, ancestral sequence reconstruction, and tracing the complex genomic histories of horizontal gene transfer.

With these tools, the broad outlines of microbial natural history have begun to emerge, but many questions remain. Has microbial diversity been shaped by the same selective processes as complex life, including mass extinctions and adaptive radiations? Have there been major successions within microbial ecological niches, with extant groups in roles previously held by extinct diversity? Does it make sense to consider such concepts as "Archean microbiota" or "Proterozoic microbiota," analogous to the major biotic transitions observed in the Phanerozoic? And how do these processes relate to the history of planetary change itself, including climate, atmosphere,

tectonics, and even impacts? Here, we provide a cursory framework that describes how interdisciplinary geobiological approaches can address these questions, propose six broadly applicable principles to aid in their investigation, and include key examples of investigations of microbial systems relating to major planetary/biogeochemical processes and events in Earth history. In doing so, we have necessarily limited our scope to microbial and molecular evolution operating within the context of a biosphere via processes observed today. Therefore, we have not extended this framework to questions of the origin of life, inclusive of prebiotic chemistry and the emergence of the earliest cells. Nevertheless, an improved understanding of microbial evolutionary history may also provide clues that can offer insight into the origin and early evolution of life on this planet.