Allometric scaling and metabolic ecology of microorganisms and major evolutionary transitions

My dissertation centers around investigating big-picture questions related to understanding the consequences of metabolism and energetics on the evolution, ecology, and physiology of life. The evolutionary transitions from prokaryotes to unicellular eukaryotes to multicellular organisms were accompanied by major innovations in metabolic design. In my first chapter, I show that the scaling of metabolic rate, population growth rate, and production efficiency with body size have changed across these transitions. Metabolic rate scales with body mass superlinearly in prokaryotes, linearly in protists, and sublinearly in metazoans, so Kleibers 3/4 power scaling law does not apply universally across organisms. This means that major changes in metabolic processes during the early evolution of life overcame existing physical constraints, exploited new opportunities, and imposed new constraints on organism physiology. Surface areas of physiological structures of organisms impose fundamental constraints on metabolic rate. In my second chapter, I demonstrate that organisms have a variety of options for increasing the scaling of the area of their metabolic surfaces with body sizes. I develop models and examples illustrating the role of cell membrane elaborations, mitochondria, vacuoles, vesicles, inclusions, and shape-shifting in the architectural design, evolution, and ecology of unicellular microbes. I demonstrate how these surface-area scaling adaptations have played important roles in the evolution of major biological designs of cells and the physiological ecology of organisms. In my third and final chapter, I integrate and synthesize findings from the previous two chapters with important developments in geochemistry, microbiology, and astrobiology in order to identify the fundamental physical and biological dimensions that characterize a metabolic theory of ecology of microorganisms. These dimensions are thermodynamics, chemical kinetics, physiological harshness, cell size, and levels of biological organization. I show how addressing these dimensions can inform understanding of the physical and biological factors governing the metabolic rate, growth rate, and geographic distribution of cells. I propose a unifying theory to understand how the major ecological and evolutionary transitions that led to increases in levels of organization of life, such as endosymbiosis, multicellularity, eusociality, and multi-domain complexes, influences the metabolism and growth and the metabolic scaling of these complexes

Global city densities: Re-examining urban scaling theory

Understanding scaling relations of social and environmental attributes of urban systems is necessary for effectively managing cities. Urban scaling theory (UST) has assumed that population density scales positively with city size. We present a new global analysis using a publicly available database of 933 cities from 38 countries. Our results showed that (18/38) 47% of countries analyzed supported increasing density scaling (pop ~ area) with exponents ~⅚ as UST predicts. In contrast, 17 of 38 countries (~45%) exhibited density scalings statistically indistinguishable from constant population densities across cities of varying sizes. These results were generally consistent in years spanning four decades from 1975 to 2015. Importantly, density varies by an order of magnitude between regions and countries and decreases in more developed economies. Our results (i) point to how economic and regional differences may affect the scaling of density with city size and (ii) show how understanding country- and region-specific strategies could inform effective management of urban systems for biodiversity, public health, conservation and resiliency from local to global scales.200 word statement of contribution: Urban Scaling Theory (UST) is a general scaling framework that makes quantitative predictions for how many urban attributes spanning physical, biological and social dimensions scale with city size; thus, UST has great implications in guiding future city developments. A major assumption of UST is that larger cities become denser. We evaluated this assumption using a publicly available global dataset of 933 cities in 38 countries. Our scaling analysis of population size and area of cities revealed that while many countries analyzed showed increasing densities with city size, about 45% of countries showed constant densities across cities. These results question a key assumption of UST. Our results suggest policies and management strategies for biodiversity conservation, public health and sustainability of urban systems may need to be tailored to national and regional scaling relations to be effective

The Macroecology of Sustainability

Global consumption rates of vital resources suggest that we have surpassed the capacity of the Earth to sustain current levels, much less future trajectories of growth in human population and economy

Data from: General models for the spectra of surface area scaling strategies of cells and organisms: fractality, geometric dissimilitude, and internalization

Surface areas and volumes of biological systems—from molecules to organelles, cells, and organisms—affect their biological rates and kinetics. Therefore, surface-area-to-volume ratios and the scaling of surface area with volume profoundly influences ecology, physiology, and evolution. The zeroth-order geometric expectation is that surface area scales with body mass or volume as a power law with an exponent of two-thirds, with consequences for surface-area-to-volume (SA:V) ratios and constraints on size; however, organisms have adaptations for altering the surface area scaling and SA:V ratios of their bodies and structures. The strategies fall into three groups: (i) fractal-like surface convolutions and crinkles; (ii) classic geometric dissimilitude through elongating, flattening, fattening, and hollowing; and (iii) internalization of surfaces. Here I develop general quantitative theory to model the spectra of effects of these strategies on SA:V ratios and surface area scaling, from exponents of less than two-thirds to superlinear scaling and mixed-power laws. Applying the theory to cells helps quantitatively evaluate the effects of membrane fractality, shape-shifting, vacuoles, vesicles, and mitochondria on surface area scaling, informing understanding of cell allometry, morphology, and evolution. Analysis of compiled data indicates that through hollowness and surface internalization eukaryotic phytoplankton increase their effective surface area scaling, attaining near-linear scaling in larger cells. This unifying theory highlights the fundamental role of biological surfaces in metabolism and morphological evolution

Scaling of total vacuolar volume with non-vacuolar cell volume in eukaryotic phytoplankton

Data include vacuolar and cell volumes for 21 species of phytoplankton

Metabolic compatibility and the rarity of prokaryote endosymbioses

The evolution of the mitochondria was a significant event that gave rise to the eukaryotic lineage and most large complex life. Central to the origins of the mitochondria was an endosymbiosis between prokaryotes. Yet, despite the potential benefits that can stem from a prokaryotic endosymbiosis, their modern occurrence is exceptionally rare. While many factors may contribute to their rarity, we lack methods for estimating the extent to which they constrain the appearance of a prokaryotic endosymbiosis. Here, we address this knowledge gap by examining the role of metabolic compatibility between a prokaryotic host and endosymbiont. We use genome-scale metabolic flux models from three different collections (AGORA, KBase, and CarveMe) to assess the viability, fitness, and evolvability of potential prokaryotic endosymbioses. We find that while more than half of host-endosymbiont pairings are metabolically viable, the resulting endosymbioses have reduced growth rates compared to their ancestral metabolisms and are unlikely to gain mutations to overcome these fitness differences. In spite of these challenges, we do find that they may be more robust in the face of environmental perturbations at least in comparison with the ancestral host metabolism lineages. Our results provide a critical set of null models and expectations for understanding the forces that shape the structure of prokaryotic life

The Malthusian–Darwinian dynamic and the trajectory of civilization

Two interacting forces influence all populations: the Malthusian dynamic of exponential growth until resource limits are reached, and the Darwinian dynamic of innovation and adaptation to circumvent these limits through biological and/or cultural evolution. The specific manifestations of these forces in modern human society provide an important context for determining how humans can establish a sustainable relationship with the finite Earth

Data from: Food spoilage, storage, and transport: implications for a sustainable future

Human societies have always faced temporal and spatial fluctuations in food availability. The length of time that food remains edible and nutritious depends on temperature, moisture, and other factors that affect the growth rates of organisms that cause spoilage. Some storage techniques, such as drying, salting, and smoking, date back to ancient hunter–gatherer and early agricultural societies and use relatively low energy inputs. Newer technologies developed since the industrial revolution, such as canning and compressed-gas refrigeration, require much greater energy inputs. Coincident with the development of storage technologies, the transportation of food helped to overcome spatial and temporal fluctuations in productivity, culminating in today's global transport system, which delivers fresh and preserved foods worldwide. Because most contemporary humans rely on energy-intensive technologies for storing and transporting food, there are formidable challenges for feeding a growing and increasingly urbanized global population as finite supplies of fossil fuels rapidly deplete