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.

Are size and mitochondrial power of cells inter-determined?

Mitochondria are the central hub of ATP production in most eukaryotic cells. Cellular power (energy per unit time), which is primarily generated in these organelles, is crucial to our understanding of cell function in health and disease. We investigated the relation between a mitochondrion's power (metabolic rate) and host cell size by combining metabolic theory with the analysis of two recent databases, one covering 109 protists and the other 63 species including protists, metazoans, microalgae, and vascular plants. We uncovered an interesting statistical regularity: in well-fed protists, relatively elevated values of mitochondrion power cluster around the smallest cell sizes and the medium-large cell sizes. In contrast, in starved protists and metazoans, the relation between mitochondrion power and cell size is inconclusive, and in microalgae and plants, mitochondrion power seems to increase from smaller cells to larger ones (where this investigation includes plant cells of volume up to ca. 2.18 × 105 µm3). Using these results, estimates are provided of the number of active ATP synthase molecules and basal uncouplers.

Limits to the three domains of life: lessons from community assembly along an Antarctic salinity gradient.

Extremophiles exist among all three domains of life; however, physiological mechanisms for surviving harsh environmental conditions differ among Bacteria, Archaea and Eukarya. Consequently, we expect that domain-specific variation of diversity and community assembly patterns exist along environmental gradients in extreme environments. We investigated inter-domain community compositional differences along a high-elevation salinity gradient in the McMurdo Dry Valleys, Antarctica. Conductivity for 24 soil samples collected along the gradient ranged widely from 50 to 8355 µS cm-1. Taxonomic richness varied among domains, with a total of 359 bacterial, 2 archaeal, 56 fungal, and 69 non-fungal eukaryotic operational taxonomic units (OTUs). Richness for bacteria, archaea, fungi, and non-fungal eukaryotes declined with increasing conductivity (all P < 0.05). Principal coordinate ordination analysis (PCoA) revealed significant (ANOSIM R = 0.97) groupings of low/high salinity bacterial OTUs, while OTUs from other domains were not significantly clustered. Bacterial beta diversity was unimodally distributed along the gradient and had a nested structure driven by species losses, whereas in fungi and non-fungal eukaryotes beta diversity declined monotonically without strong evidence of nestedness. Thus, while increased salinity acts as a stressor in all domains, the mechanisms driving community assembly along the gradient differ substantially between the domains.

Major evolutionary transitions of life, metabolic scaling and the number and size of mitochondria and chloroplasts.

We investigate the effects of trophic lifestyle and two types of major evolutionary transitions in individuality-the endosymbiotic acquisition of organelles and development of multicellularity-on organellar and cellular metabolism and allometry. We develop a quantitative framework linking the size and metabolic scaling of eukaryotic cells to the abundance, size and metabolic scaling of mitochondria and chloroplasts and analyse a newly compiled, unprecedented database representing unicellular and multicellular cells covering diverse phyla and tissues. Irrespective of cellularity, numbers and total volumes of mitochondria scale linearly with cell volume, whereas chloroplasts scale sublinearly and sizes of both organelles remain largely invariant with cell size. Our framework allows us to estimate the metabolic scaling exponents of organelles and cells. Photoautotrophic cells and organelles exhibit photosynthetic scaling exponents always less than one, whereas chemoheterotrophic cells and organelles have steeper respiratory scaling exponents close to one. Multicellularity has no discernible effect on the metabolic scaling of organelles and cells. In contrast, trophic lifestyle has a profound and uniform effect, and our results suggest that endosymbiosis fundamentally altered the metabolic scaling of free-living bacterial ancestors of mitochondria and chloroplasts, from steep ancestral scaling to a shallower scaling in their endosymbiotic descendants.

Niche and metabolic principles explain patterns of diversity and distribution: theory and a case study with soil bacterial communities.

The causes of biodiversity patterns are controversial and elusive due to complex environmental variation, covarying changes in communities, and lack of baseline and null theories to differentiate straightforward causes from more complex mechanisms. To address these limitations, we developed general diversity theory integrating metabolic principles with niche-based community assembly. We evaluated this theory by investigating patterns in the diversity and distribution of soil bacteria taxa across four orders of magnitude variation in spatial scale on an Antarctic mountainside in low complexity, highly oligotrophic soils. Our theory predicts that lower temperatures should reduce taxon niche widths along environmental gradients due to decreasing growth rates, and the changing niche widths should lead to contrasting α- and ß-diversity patterns. In accord with the predictions, α-diversity, niche widths and occupancies decreased while ß-diversity increased with increasing elevation and decreasing temperature. The theory also successfully predicts a hump-shaped relationship between α-diversity and pH and a negative relationship between α-diversity and salinity. Thus, a few simple principles explained systematic microbial diversity variation along multiple gradients. Such general theory can be used to disentangle baseline effects from more complex effects of temperature and other variables on biodiversity patterns in a variety of ecosystems and organisms.

The macroecology of sustainability.

The discipline of sustainability science has emerged in response to concerns of natural and social scientists, policymakers, and lay people about whether the Earth can continue to support human population growth and economic prosperity. Yet, sustainability science has developed largely independently from and with little reference to key ecological principles that govern life on Earth. A macroecological perspective highlights three principles that should be integral to sustainability science: 1) physical conservation laws govern the flows of energy and materials between human systems and the environment, 2) smaller systems are connected by these flows to larger systems in which they are embedded, and 3) global constraints ultimately limit flows at smaller scales. Over the past few decades, decreasing per capita rates of consumption of petroleum, phosphate, agricultural land, fresh water, fish, and wood indicate that the growing human population has surpassed the capacity of the Earth to supply enough of these essential resources to sustain even the current population and level of socioeconomic development.

The maximum rate of mammal evolution.

How fast can a mammal evolve from the size of a mouse to the size of an elephant? Achieving such a large transformation calls for major biological reorganization. Thus, the speed at which this occurs has important implications for extensive faunal changes, including adaptive radiations and recovery from mass extinctions. To quantify the pace of large-scale evolution we developed a metric, clade maximum rate, which represents the maximum evolutionary rate of a trait within a clade. We applied this metric to body mass evolution in mammals over the last 70 million years, during which multiple large evolutionary transitions occurred in oceans and on continents and islands. Our computations suggest that it took a minimum of 1.6, 5.1, and 10 million generations for terrestrial mammal mass to increase 100-, and 1,000-, and 5,000-fold, respectively. Values for whales were down to half the length (i.e., 1.1, 3, and 5 million generations), perhaps due to the reduced mechanical constraints of living in an aquatic environment. When differences in generation time are considered, we find an exponential increase in maximum mammal body mass during the 35 million years following the Cretaceous-Paleogene (K-Pg) extinction event. Our results also indicate a basic asymmetry in macroevolution: very large decreases (such as extreme insular dwarfism) can happen at more than 10 times the rate of increases. Our findings allow more rigorous comparisons of microevolutionary and macroevolutionary patterns and processes.

Patterns of maximum body size evolution in Cenozoic land mammals: eco-evolutionary processes and abiotic forcing.

There is accumulating evidence that macroevolutionary patterns of mammal evolution during the Cenozoic follow similar trajectories on different continents. This would suggest that such patterns are strongly determined by global abiotic factors, such as climate, or by basic eco-evolutionary processes such as filling of niches by specialization. The similarity of pattern would be expected to extend to the history of individual clades. Here, we investigate the temporal distribution of maximum size observed within individual orders globally and on separate continents. While the maximum size of individual orders of large land mammals show differences and comprise several families, the times at which orders reach their maximum size over time show strong congruence, peaking in the Middle Eocene, the Oligocene and the Plio-Pleistocene. The Eocene peak occurs when global temperature and land mammal diversity are high and is best explained as a result of niche expansion rather than abiotic forcing. Since the Eocene, there is a significant correlation between maximum size frequency and global temperature proxy. The Oligocene peak is not statistically significant and may in part be due to sampling issues. The peak in the Plio-Pleistocene occurs when global temperature and land mammal diversity are low, it is statistically the most robust one and it is best explained by global cooling. We conclude that the macroevolutionary patterns observed are a result of the interplay between eco-evolutionary processes and abiotic forcing.

Soil microbial responses to increased moisture and organic resources along a salinity gradient in a polar desert.

Microbial communities in extreme environments often have low diversity and specialized physiologies suggesting a limited resistance to change. The McMurdo Dry Valleys (MDV) are a microbially dominated, extreme ecosystem currently undergoing climate change-induced disturbances, including the melting of massive buried ice, cutting through of permafrost by streams, and warming events. These processes are increasing moisture across the landscape, altering conditions for soil communities by mobilizing nutrients and salts and stimulating autotrophic carbon inputs to soils. The goal of this study was to determine the effects of resource addition (water/organic matter) on the composition and function of microbial communities in the MDV along a natural salinity gradient representing an additional gradient of stress in an already extreme environment. Soil respiration and the activity of carbon-acquiring extracellular enzymes increased significantly (P < 0.05) with the addition of resources at the low- and moderate-salinity sites but not the high-salinity site. The bacterial community composition was altered, with an increase in Proteobacteria and Firmicutes with water and organic matter additions at the low- and moderate-salinity sites and a near dominance of Firmicutes at the high-salinity site. Principal coordinate analyses of all samples using a phylogenetically informed distance matrix (UniFrac) demonstrated discrete clustering among sites (analysis of similarity [ANOSIM], P < 0.05 and R > 0.40) and among most treatments within sites. The results from this experimental work suggest that microbial communities in this environment will undergo rapid change in response to the altered resources resulting from climate change impacts occurring in this region.

Macroecology Meets Macroeconomics: Resource Scarcity and Global Sustainability.

The current economic paradigm, which is based on increasing human population, economic development, and standard of living, is no longer compatible with the biophysical limits of the finite Earth. Failure to recover from the economic crash of 2008 is not due just to inadequate fiscal and monetary policies. The continuing global crisis is also due to scarcity of critical resources. Our macroecological studies highlight the role in the economy of energy and natural resources: oil, gas, water, arable land, metals, rare earths, fertilizers, fisheries, and wood. As the modern industrial technological-informational economy expanded in recent decades, it grew by consuming the Earth's natural resources at unsustainable rates. Correlations between per capita GDP and per capita consumption of energy and other resources across nations and over time demonstrate how economic growth and development depend on "nature's capital". Decades-long trends of decreasing per capita consumption of multiple important commodities indicate that overexploitation has created an unsustainable bubble of population and economy.

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 influence 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: (1) fractal-like surface convolutions and crinkles; (2) classic geometric dissimilitude through elongating, flattening, fattening, and hollowing; and (3) 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.

Effects of allometry, productivity and lifestyle on rates and limits of body size evolution.

Body size affects nearly all aspects of organismal biology, so it is important to understand the constraints and dynamics of body size evolution. Despite empirical work on the macroevolution and macroecology of minimum and maximum size, there is little general quantitative theory on rates and limits of body size evolution. We present a general theory that integrates individual productivity, the lifestyle component of the slow-fast life-history continuum, and the allometric scaling of generation time to predict a clade's evolutionary rate and asymptotic maximum body size, and the shape of macroevolutionary trajectories during diversifying phases of size evolution. We evaluate this theory using data on the evolution of clade maximum body sizes in mammals during the Cenozoic. As predicted, clade evolutionary rates and asymptotic maximum sizes are larger in more productive clades (e.g. baleen whales), which represent the fast end of the slow-fast lifestyle continuum, and smaller in less productive clades (e.g. primates). The allometric scaling exponent for generation time fundamentally alters the shape of evolutionary trajectories, so allometric effects should be accounted for in models of phenotypic evolution and interpretations of macroevolutionary body size patterns. This work highlights the intimate interplay between the macroecological and macroevolutionary dynamics underlying the generation and maintenance of morphological diversity.

Shifts in metabolic scaling, production, and efficiency across major evolutionary transitions of life.

The diversification of life involved enormous increases in size and complexity. The evolutionary transitions from prokaryotes to unicellular eukaryotes to metazoans were accompanied by major innovations in metabolic design. Here we show that the scalings of metabolic rate, population growth rate, and production efficiency with body size have changed across the evolutionary transitions. Metabolic rate scales with body mass superlinearly in prokaryotes, linearly in protists, and sublinearly in metazoans, so Kleiber's 3/4 power scaling law does not apply universally across organisms. The scaling of maximum population growth rate shifts from positive in prokaryotes to negative in protists and metazoans, and the efficiency of production declines across these groups. Major changes in metabolic processes during the early evolution of life overcame existing constraints, exploited new opportunities, and imposed new constraints.

Niches, body sizes, and the disassembly of mammal communities on the Sunda Shelf islands.

The rising sea level at the end of the Pleistocene that created the islands of the Sunda Shelf in Indonesia and Malaysia provides a natural experiment in community disassembly and offers insights into the effects of body size and niches on abundance, distribution, and diversity. Since isolation, terrestrial mammal communities of these islands have been reduced by extinction, with virtually no offsetting colonization. We document three empirical patterns of disassembly, all of which are significantly different from null models of random assembly: (i) a diversity-area relationship: the number of taxa is strongly and positively correlated with island area; (ii) nested subset composition: species that occur on small islands tend to be subsets of more diverse communities inhabiting larger islands; and (iii) body size distributions: species of intermediate body sizes occur on the greatest number of islands, and smaller islands have smaller ranges of body sizes, caused by the absence of species of both very large and extremely small size. These patterns reveal the role of body size and other niche characteristics, such as habitat requirements and trophic status, in the differential susceptibility of taxa to extinction.

Contrasting trait responses in plant communities to experimental and geographic variation in precipitation.

• Patterns of precipitation are likely to change significantly in the coming century, with important but poorly understood consequences for plant communities. Experimental and correlative studies may provide insight into expected changes, but little research has addressed the degree of concordance between these approaches. • We synthesized results from four experimental water addition studies with a correlative analysis of community changes across a large natural precipitation gradient in the United States. We investigated whether community composition, summarized with plant functional traits, responded similarly to increasing precipitation among studies and sites. • In field experiments, increased precipitation favored species with small seed size, short leaf life span and high leaf nitrogen (N) concentration. However, with increasing precipitation along the natural gradient, community composition shifted towards species with higher mean seed mass, longer leaf life span and lower leaf N concentrations. • The differences in temporal and spatial scale of experimental manipulations and natural gradients may explain these contrasting results. Our results highlight the complexity of responses to climate change, and suggest that transient dynamics may not reflect long-term shifts in functional diversity and community composition. We propose a model of community change that incorporates these differences between short- and long-term responses to climate change.

Genomic adaptations in information processing underpin trophic strategy in a whole-ecosystem nutrient enrichment experiment.

Several universal genomic traits affect trade-offs in the capacity, cost, and efficiency of the biochemical information processing that underpins metabolism and reproduction. We analyzed the role of these traits in mediating the responses of a planktonic microbial community to nutrient enrichment in an oligotrophic, phosphorus-deficient pond in Cuatro Ciénegas, Mexico. This is one of the first whole-ecosystem experiments to involve replicated metagenomic assessment. Mean bacterial genome size, GC content, total number of tRNA genes, total number of rRNA genes, and codon usage bias in ribosomal protein sequences were all higher in the fertilized treatment, as predicted on the basis of the assumption that oligotrophy favors lower information-processing costs whereas copiotrophy favors higher processing rates. Contrasting changes in trait variances also suggested differences between traits in mediating assembly under copiotrophic versus oligotrophic conditions. Trade-offs in information-processing traits are apparently sufficiently pronounced to play a role in community assembly because the major components of metabolism-information, energy, and nutrient requirements-are fine-tuned to an organism's growth and trophic strategy.

Local and Regional Scale Heterogeneity Drive Bacterial Community Diversity and Composition in a Polar Desert.

The distribution of organisms in an environment is neither uniform nor random but is instead spatially patterned. The factors that control this patterning are complex and the underlying mechanisms are poorly understood. Soil microbes are critical to ecosystem function but exhibit highly complex distributions and community dynamics due in large part to the scale-dependent effects of environmental heterogeneity. To better understand the impact of environmental heterogeneity on the distribution of soil microbes, we sequenced the 16S rRNA gene from bacterial communities in the microbe-dominated polar desert ecosystem of the McMurdo Dry Valleys (MDV), Antarctica. Significant differences in key edaphic variables and alpha diversity were observed among the three lake basins of the Taylor Valley (Kruskal-Wallis; pH: χ2 = 68.89, P < 0.001, conductivity: χ2 = 35.03, P < 0.001, observed species: χ2 = 7.98, P = 0.019 and inverse Simpson: χ2 = 18.52, P < 0.001) and each basin supported distinctive microbial communities (ANOSIM R = 0.466, P = 0.001, random forest ratio of 14.1). However, relationships between community structure and edaphic characteristics were highly variable and contextual, ranging in magnitude and direction across regional, basin, and local scales. Correlations among edaphic factors (pH and soil conductivity) and the relative abundance of specific phyla were most pronounced along local environmental gradients in the Lake Fryxell basin where Acidobacteria, Bacteroidetes, and Proteobacteria declined while Deinococcus-Thermus and Gemmatimonadetes increased with soil conductivity (all P < 0.1). Species richness was most strongly related to the soil conductivity gradient present within this study system. We suggest that the relative importance of pH versus soil conductivity in structuring microbial communities is related to the length of edaphic gradients and the spatial scale of sampling. These results highlight the importance of conducting studies over large ranges of key environmental gradients and across multiple spatial scales to assess the influence of environmental heterogeneity on the composition and diversity of microbial communities.

Characterization of growing bacterial populations in McMurdo Dry Valley soils through stable isotope probing with (18) O-water.

Soil microbial communities of the McMurdo Dry Valleys, Antarctica (MDV) contain representatives from at least fourteen bacterial phyla. However, given low rates of microbial activity, it is unclear whether this richness represents functioning rather than dormant members of the community. We used stable isotope probing (SIP) with (18) O-water to determine if microbial populations grow in MDV soils. Changes in the microbial community were characterized in soils amended with H2 (18) O and H2 (18) O-organic matter. Sequencing the 16S rRNA genes of the heavy and light fractions of the bacterial community DNA shows that DNA of microbial populations was labeled with (18) O-water, indicating these micro-organisms grew in the MDV soils. Significant differences existed in the community composition of the heavy and light fractions of the H2 (18) O and H2 (18) O-organic matter amended samples (Anosim P < 0.05 of weighted Unifrac distance). Control samples and the light DNA fraction of the H2 (18) O amended samples were dominated by representatives of the phyla Deinococcus-Thermus, Proteobacteria, Planctomyces, Gemmatimonadetes, Actinobacteria and Acidobacteria, whereas Proteobacteria were more prevalent in the heavy DNA fractions from the H2 (18) O-water and the H2 (18) O-water-organic matter treatments. Our results indicate that SIP with H2 (18) O can be used to distinguish active bacterial populations even in this low organic matter environment.

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.