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Risk–reward trade-off during carbon starvation generates dichotomy in motility endurance among marine bacteria
Abstract
Copiotrophic marine bacteria contribute to the control of carbon storage in the ocean by remineralizing organic matter. Motility presents copiotrophs with a risk–reward trade-of: it is highly benefcial in seeking out sparse nutrient hotspots, but energetically costly. Here we studied the motility endurance of 26 marine isolates, representing 18 species, using video microscopy and cell tracking over 2 days of carbon starvation. We found that the trade-of results in a dichotomy among marine bacteria, in which risk-averse copiotrophs ceased motility within hours (‘limostatic’), whereas risk-prone copiotrophs converted ~9% of their biomass per day into energy to retain motility for the 2 days of observation (‘limokinetic’). Using machine learning classifers, we identifed a genomic component associated with both strategies, sufciently robust to predict the response of additional species with 86% accuracy. This dichotomy can help predict the prevalence of foraging strategies in marine microbes and inform models of ocean carbon cycles.
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Functional biogeography of marine microbial heterotrophs
Abstract
Heterotrophic bacteria and archaea (“heteroprokaryotes”) drive global carbon cycling, but how to quantitatively organize their functional complexity remains unclear. We generated a global-scale understanding of marine heteroprokaryotic functional biogeography by synthesizing genetic sequencing data with a mechanistic marine ecosystem model. We incorporated heteroprokaryotic diversity into the trait-based model along two axes: substrate lability and growth strategy. Using genetic sequences along three ocean transects, we compiled 21 heteroprokaryotic guilds and estimated their degree of optimization for rapid growth (copiotrophy). Data and model consistency indicated that gradients in grazing and substrate lability predominantly set biogeographical patterns, and we identified deep-ocean “slow copiotrophs” whose ecological interactions control the surface accumulation of dissolved organic carbon.
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Distantly related bacteria share a rigid proteome allocation strategy with flexible enzyme kinetics
Abstract
Bacteria are known to allocate their proteomes according to how fast they grow, and the allocation strategies employed strongly affect bacterial adaptation to different environments. Much of what is currently known about proteome allocation is based on extensive studies of the model organism Escherichia coli. It is not clear how much of E. coli’s proteome allocation strategy is applicable to other species, particularly since different species can grow at vastly different rates even in the same growth condition. In this study, we investigate differences in nutrient-dependent proteome allocation programs adopted by several distantly related bacterial species, including Vibrio natriegens, one of the fastest-growing bacteria known. Extensive quantitative proteome characterization across conditions reveals an invariant allocation program in response to changing nutrients despite systemic, species-specific differences in enzyme kinetics. This invariant program is not organized according to the growth rate but is based on a common internal metric of nutrient quality after scaling away species-specific differences in enzyme kinetics, with the faster species behaving as if it is growing under a higher temperature. The flexibility of enzyme kinetics and the rigidity of proteome allocation programs across species defy common notions of evolvability and resource optimization. Our results suggest the existence of a blueprint of proteome allocation shared by diverse bacterial species, with implications on common underlying regulatory strategies. Further knowledge on the existence and organization of such phylogeny-transcending relations also promises to simplify the bottom–up description and understanding of bacterial behaviors in ecological communities.
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Dynamic coexistence driven by physiological transitions in microbial communities
Abstract
Microbial ecosystems are commonly modeled by fixed interactions between species in steady exponential growth states. However, microbes in exponential growth often modify their environments so strongly that they are forced out of the growth state into stressed, nongrowing states. Such dynamics are typical of ecological succession in nature and serial-dilution cycles in the laboratory. Here, we introduce a phenomenological model, the Community State Model, to gain insight into the dynamic coexistence of microbes due to changes in their physiological states during cyclic succession. Our model specifies the growth preference of each species along a global ecological coordinate, taken to be the biomass density of the community, but is otherwise agnostic to specific interactions (e.g., nutrient starvation, stress, aggregation), in order to focus on self-consistency conditions on combinations of physiological states, “community states,” in a stable ecosystem. We identify three key features of such dynamical communities that contrast starkly with steady-state communities: enhanced community stability through staggered dominance of different species in different community states, increased tolerance of community diversity to fast growing species dominating distinct community states, and increased requirement of growth dominance by late-growing species. These features, derived explicitly for simplified models, are proposed here as principles aiding the understanding of complex dynamical communities. Our model shifts the focus of ecosystem dynamics from bottom–up studies based on fixed, idealized interspecies interaction to top–down studies based on accessible macroscopic observables such as growth rates and total biomass density, enabling quantitative examination of community-wide characteristics.
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Clear as mud redefined: Tunable transparent mineral scaffolds for visualizing microbial processes below ground
Abstract
Microbes inhabiting complex porous microenvironments in sediments and aquifers catalyze reactions that are critical to global biogeochemical cycles and ecosystem health. However, the opacity and complexity of porous sediment and rock matrices have considerably hindered the study of microbial processes occurring within these habitats. Here, we generated microbially compatible, optically transparent mineral scaffolds to visualize and investigate microbial colonization and activities occurring in these environments, in laboratory settings and in situ. Using inexpensive synthetic cryolite mineral, we produced optically transparent scaffolds mimicking the complex 3D structure of sediments and rocks by adapting a suspension-based, freeze-casting technique commonly used in materials science. Fine-tuning of parameters, such as freezing rate and choice of solvent, provided full control of pore size and architecture. The combined effects of scaffold porosity and structure on the movement of microbe-sized particles, tested using velocity tracking of fluorescent beads, showed diverse yet reproducible behaviors. The scaffolds we produced are compatible with epifluorescence microscopy, allowing the fluorescence-based identification of colonizing microbes by DNA-based staining and fluorescence in situ hybridization (FISH) to depths of 100 µm. Additionally, Raman spectroscopy analysis indicates minimal background signal in regions used for measuring deuterium and 13C enrichment in microorganisms, highlighting the potential to directly couple D2O or 13C stable isotope probing and Raman-FISH for quantifying microbial activity at the single-cell level. To demonstrate the relevance of cryolite scaffolds for environmental field studies, we visualized their colonization by diverse microorganisms within rhizosphere sediments of a coastal seagrass plant using epifluorescence microscopy. The tool presented here enables highly resolved, spatially explicit, and multimodal investigations into the distribution, activities, and interactions of underground microbes typically obscured within opaque geological materials until now.
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Biogel scavenging slows the sinking of organic particles to the ocean depths
Abstract
One of Earth’s largest carbon fluxes is driven by particles made from photosynthetically fixed matter, which aggregate and sink into the deep ocean. While biodegradation is known to reduce this vertical flux, the biophysical processes that control particle sinking speed are not well understood. Here, we use a vertical millifluidic column to video-track single particles and find that biogels scavenged by particles during sinking significantly reduce the particles’ sinking speed, slowing them by up to 45% within one day. Combining observations with a mathematical model, we determine that the mechanism for this slowdown is a combination of increased drag due to the formation of biogel tendrils and increased buoyancy due to the biogel’s low density. Because biogels are pervasive in the ocean, we propose that by slowing the sinking of organic particles they attenuate the vertical carbon flux in the ocean.
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Replicating community dynamics reveals how initial composition shapes the functional outcomes of bacterial communities
Abstract
Bacterial communities play key roles in global biogeochemical cycles, industry, agriculture, human health, and animal husbandry. There is therefore great interest in understanding bacterial community dynamics so that they can be controlled and engineered to optimise ecosystem services. We assess the
reproducibility and predictability of bacterial community dynamics by creating a frozen archive of hundreds of naturally-occurring bacterial communities that we repeatedly revive and track in a standardised, complex resource environment. Replicate communities follow reproducible trajectories and the community dynamics closely map to ecosystem functioning. However, even under standardised conditions, the communities exhibit tipping-points, where small differences in initial community composition create divergent compositional and functional outcomes. The predictability of community trajectories therefore requires detailed knowledge of rugged compositional landscapes
where ecosystem properties are not the inevitable result of prevailing environmental conditions but can be tilted toward different outcomes depending on the initial community composition. Our results shed light on the relationship between composition and function, opening new avenues to understand
the feasibility and limitations of function prediction in complex microbial communities. -
Disentangling the feedback loops driving spatial patterning in microbial communities
Abstract
The properties of multispecies biofilms are determined by how species are arranged in space. How these patterns emerge is a complex and largely unsolved problem. Here, we synthesize the known factors affecting pattern formation, identify the interdependencies and feedback loops coupling them, and discuss approaches to disentangle their effects. Finally, we propose an interdisciplinary research program that could create a predictive understanding of pattern formation in microbial communities.
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Microbial Ecology to Ocean Carbon Cycling: From Genomes to Numerical Models
Abstract
The oceans contain large reservoirs of inorganic and organic carbon and play a critical role in both global carbon cycling and climate. Most of the biogeochemical transformations in the oceans are driven by marine microbes. Thus, molecular processes occurring at the scale of single cells govern global geochemical dynamics, posing a challenge of scales. Understanding the processes controlling ocean carbon cycling from the cellular to the global scale requires the integration of multiple disciplines including microbiology, ecology, biogeochemistry, and computational fields such as numerical models and bioinformatics. A shared language and foundational knowledge will facilitate these interactions. This review provides the state of knowledge on the role marine microbes play in large-scale ocean carbon cycling through the lens of observational oceanography and biogeochemical models. We conclude by outlining ways in which the field can bridge the gap between -omics datasets and ocean models to understand ocean carbon cycling across scales.
- -Omic approaches are providing increasingly quantitative insight into the biogeochemical functions of marine microbial ecosystems.
- Numerical models provide a tool for studying global carbon cycling by scaling from the microscale to the global scale.
- The integration of -omics and numerical modeling generates new understanding of how microbial metabolisms and community dynamics set nutrient fluxes in the ocean.
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Mechanistic Insights Into Post-Translational α-Keto-β-Amino Acid Formation by a Radical S-Adenosyl Methionine Peptide Splicease
Abstract
Radical S-adenosyl methionine enzymes catalyze a diverse repertoire of post-translational modifications in protein and peptide substrates. Among these, an exceptional and mechanistically obscure example is the installation of α-keto-β-amino acid residues by formal excision of a tyrosine-derived tyramine unit. The responsible spliceases are key maturases in a widespread family of natural products termed spliceotides that comprise potent protease inhibitors, with the installed β-residues
being crucial for bioactivity. Here, we established the in vitro activity of the model splicease PcpXY to interrogate the mechanism of non-canonical protein splicing. Identification of shunt and coproducts, deuterium labeling studies, and density functional theory energy calculations of hypothesized intermediates support a mechanism involving hydrogen abstraction at tyrosine Cα as the initial site of peptide radical formation and release of 4-hydroxybenzaldehyde as the tyrosine-derived coproduct. The data illuminate key features of this unprecedented radical-mediated biotransformation yielding ketoamide pharmacophores that are also present in peptidomimetic therapeutics. -
Slower swimming promotes chemotactic encounters between bacteria and small phytoplankton
Abstract
Chemotaxis enables marine bacteria to increase encounters with phytoplankton cells by reducing their search times, provided that bacteria detect noisy chemical gradients around phytoplankton. Gradient detection depends on bacterial phenotypes and phytoplankton size: large phytoplankton produce spatially extended but shallow gradients, whereas small phytoplankton produce steeper but spatially more confined gradients. To date, it has remained unclear how phytoplankton size and bacterial swimming speed affect bacteria’s gradient detection ability and search times for phytoplankton. Here, we compute an upper bound on the increase in bacterial encounter rate with phytoplankton due to chemotaxis over random motility alone. We find that chemotaxis can substantially decrease search times for small phytoplankton, but this advantage is highly sensitive to variations in bacterial phenotypes or phytoplankton leakage rates. By contrast, chemotaxis toward large phytoplankton cells reduces the search time more modestly, but this benefit is more robust to variations in search or environmental parameters. Applying our findings to marine phytoplankton communities, we find that, in productive waters, chemotaxis toward phytoplankton smaller than 2 μm provides little to no benefit, but can decrease average search times for large phytoplankton (∼20 μm) from 2 wk to 2 d, an advantage that is robust to variations and favors bacteria with higher swimming speeds. By contrast, in oligotrophic waters, chemotaxis can reduce search times for picophytoplankton (∼1 μm) up to 10-fold, from a week to half a day, but only for bacteria with low swimming speeds and long sensory timescales. This asymmetry may promote the coexistence of diverse search phenotypes in marine bacterial populations.