Maureen A. O'Malley

Varieties of Living Things: Life at the Intersection of Lineage and Metabolism

We address three fundamental questions: What does it mean for an entity to be living? What is the role of inter-organismic collaboration in evolution? What is a biological individual? Our central argument is that life arises when lineage-forming entities collaborate in metabolism. By conceiving of metabolism as a collaborative process performed by functional wholes, which are associations of a variety of lineage-forming entities, we avoid the standard tension between reproduction and metabolism in discussions of life – a tension particularly evident in discussions of whether viruses are alive. Our perspective assumes no sharp distinction between life and non-life, and does not equate life exclusively with cellular or organismal status. We reach this conclusion through an analysis of the capabilities of a spectrum of biological entities, in which we include the pivotal case of viruses as well as prions, plasmids, organelles, intracellular and extracellular symbionts, unicellular and multicellular life forms. The usual criterion for classifying many of the entities of our continuum as non-living is autonomy. This emphasis on autonomy is problematic, however, because even paradigmatic biological individuals, such as large animals, are dependent on symbiotic associations with many other organisms. These composite individuals constitute the metabolic wholes on which selection acts. Finally, our account treats cooperation and competition not as polar opposites but as points on a continuum of collaboration. We suggest that competitive relations are a transitional state, with multi-lineage metabolic wholes eventually outcompeting selfish competitors, and that this process sometimes leads to the emergence of new types or levels of wholes. Our view of life as a continuum of variably structured collaborative systems leaves open the possibility that a variety of forms of organized matter – from chemical systems to ecosystems – might be usefully understood as living entities.

How stands the Tree of Life a century and a half after The Origin

We examine the Tree of Life (TOL) as an evolutionary hypothesis and a heuristic. The original TOL hypothesis has failed but a new statistical TOL hypothesis is promising. The TOL heuristic usefully organizes data without positing fundamental evolutionary truth.ReviewersThis article was reviewed by W. Ford Doolittle, Nicholas Galtier and Christophe Malaterre.

Enlightening the life sciences: the history of halobacterial and microbial rhodopsin research

The history of research on microbial rhodopsins offers a novel perspective on the history of the molecular life sciences. Events in this history play important roles in the development of fields such as general microbiology, membrane research, bioenergetics, metagenomics and, very recently, neurobiology. New concepts, techniques, methods and fields have arisen as a result of microbial rhodopsin investigations. In addition, the history of microbial rhodopsins sheds light on the dynamic connections between basic and applied science, and hypothesis-driven and data-driven approaches. The story begins with the late nineteenth century discovery of microorganisms on salted fish and leads into ecological and taxonomical studies of halobacteria in hypersaline environments. These programmes were built on by the discovery of bacteriorhodopsin in organisms that are part of what is now known as the archaeal genus Halobacterium. The transfer of techniques from bacteriorhodopsin studies to the metagenomic discovery of proteorhodopsin in 2000 further extended the field. Microbial rhodopsins have also been used as model systems to understand membrane protein structure and function, and they have become the target of technological applications such as optogenetics and nanotechnology. Analysing the connections between these historical episodes provides a rich example of how science works over longer time periods, especially with regard to the transfer of materials, methods and concepts between different research fields.

Evolutionary systems biology: What it is and why it matters

Evolutionary systems biology (ESB) is a rapidly growing integrative approach that has the core aim of generating mechanistic and evolutionary understanding of genotype‐phenotype relationships at multiple levels. ESBs more specific objectives include extending knowledge gained from model organisms to non‐model organisms, predicting the effects of mutations, and defining the core network structures and dynamics that have evolved to cause particular intracellular and intercellular responses. By combining mathematical, molecular, and cellular approaches to evolution, ESB adds new insights and methods to the modern evolutionary synthesis, and offers ways in which to enhance its explanatory and predictive capacities. This combination of prediction and explanation marks ESB out as a research manifesto that goes further than its two contributing fields. Here, we summarize ESB via an analysis of characteristic research examples and exploratory questions, while also making a case for why these integrative efforts are worth pursuing.

How Do Microbial Populations and Communities Function as Model Systems

Microbial model systems have made major contributions across the life sciences. Their influence extends beyond strictly microbiological research to inform and enhance general biological understanding. To cast light on how microbial populations and communities function as model systems, we examine their use in historical and contemporary research on evolutionary and ecological dynamics. We assess the pros and cons of microbial model systems, and identify specific ways in which they benefit research. Analyzing microbial model systems is of particular value as biologists become increasingly aware of the microbial world and its interactions with the rest of life.

Multilevel Research Strategies and Biological Systems

Multilevel research strategies characterize contemporary molecular inquiry into biological systems. We outline conceptual, methodological, and explanatory dimensions of these multilevel strategies in microbial ecology, systems biology, protein research, and developmental biology. This review of emerging lines of inquiry in these fields suggests that multilevel research in molecular life sciences has significant implications for philosophical understandings of explanation, modeling, and representation.

The ecological virus

Ecology is usually described as the study of organisms interacting with one another and their environments. From this view of ecology, viruses - not usually considered to be organisms - would merely be part of the environment. Since the late 1980s, however, a growing stream of micrographic, experimental, molecular, and model-based (theoretical) research has been investigating how and why viruses should be understood as ecological actors of the most important sort. Viruses, especially phage, have been revealed as participants in the planets most crucial food webs, even though viruses technically consume nothing (they do not metabolize by themselves). Even more impressively, viruses have been identified as regulators of planetary biogeochemistry, in which they control cycles such as carbon, nitrogen and phosphorus - cycles on which all life depends. Although much biogeochemical research black-boxes the entities filling functional roles, it is useful to focus a little more closely to understand how viruses can be held responsible for the global processes of life. This paper will give a brief overview of the history of virus ecology and tease out the implications of large-scale ecological modelling with viruses. This analysis suggests that viruses should be conceptualized as ecological actors that are at least comparable and possibly equal to organismal actors. Ecological agency can therefore be distinguished from standard interpretations of biological agency.

Histories of molecules: Reconciling the past.

Molecular data and methods have become centrally important to evolutionary analysis, largely because they have enabled global phylogenetic reconstructions of the relationships between organisms in the tree of life. Often, however, molecular stories conflict dramatically with morphology-based histories of lineages. The evolutionary origin of animal groups provides one such case. In other instances, different molecular analyses have so far proved irreconcilable. The ancient and major divergence of eukaryotes from prokaryotic ancestors is an example of this sort of problem. Efforts to overcome these conflicts highlight the role models play in phylogenetic reconstruction. One crucial model is the molecular clock; another is that of simple-to-complex modification. I will examine animal and eukaryote evolution against a backdrop of increasing methodological sophistication in molecular phylogeny, and conclude with some reflections on the nature of historical science in the molecular era of phylogeny.

Microbiology, Philosophy, and Education

There are not only many links between microbiological and philosophical topics, but good educational reasons for microbiologists to explore the philosophical issues in their fields. I examine three broad issues of classification, causality and model systems, showing how these philosophical dimensions have practical implications. I conclude with a discussion of the educational benefits for recognising the philosophy in microbiology.

Microbes, mathematics, and models

Microbial model systems have a long history of fruitful use in fields that include evolution and ecology. In order to develop further insight into modelling practice, we examine how the competitive exclusion and coexistence of competing species have been modelled mathematically and materially over the course of a long research history. In particular, we investigate how microbial models of these dynamics interact with mathematical or computational models of the same phenomena. Our cases illuminate the ways in which microbial systems and equations work as models, and what happens when they generate inconsistent findings about shared targets. We reveal an iterative strategy of comparative modelling in different media, and suggest reasons why microbial models have a special degree of epistemic tractability in multimodel inquiry.