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Cordero, O. X.

Publications and source records attributed to Cordero, O. X..

At least 19 recordsLinked to original sources

Niche partitioning by resource size in the gut microbiome

Niche partitioning promotes diversity of the human gut microbiota. However, the molecular basis of resource specialization and niche separation in the gut remains poorly understood. Here we show that structural differences in glycan transporters drive members of the genus Bacteroides, common human gut commensals, to specialize on distinct chain lengths of the same fructan molecule. While species encoding canonical SusCD systems for glycan import -formed by a membrane-embedded barrel capped with a lipoprotein lid- specialized in long-chain fructans, species with smaller lidless transporters, not previously described in Bacteroides, specialized in short-chain fructans. Strikingly, we found that a [~]140-amino acid domain in the SusC barrel is a structural feature that governs substrate preference: deleting it does not impair transport but instead shifts uptake preferences from long-to short-chain fructans. These structural differences predict competitive outcomes in vivo on fructans of varying lengths, suggesting that glycan uptake mechanisms shape ecological niches in the gut and can inform fiber-based dietary interventions. Similar small lidless transporters exist across the Bacteroidota, expanding the paradigm of glycan utilization in this phylum beyond the canonical SusCD architecture.

microbiology↗

A universal surface functionalization technique to chemically enhance live microbial cells

Microbial surface functionalization is a powerful strategy for endowing microbes with novel, non-genetic functions. However, existing methods are often species-specific, limited in scope, and compromise cell viability. Here, we present a universal and modular platform for high-density, reproducible surface functionalization across diverse microbial species--including Gram-positive, Gram-negative, aerobic, and anaerobic bacteria--using multiple molecular classes such as fluorophores, enzymes, and nucleic acids. Our method preserves cell viability, and achieves 50x higher functionalization efficiency than previous methods with a standardized protocol applicable to any azide-containing molecule. Applications of the method show reproducible and tunable phenotypic outcomes at the single-cell level: fluorophore labeling yielded adjustable fluorescence, {beta}-lactamase conferred scalable antibiotic resistance, and DNA coatings modulated adhesion and aggregation. This platform provides quantitative, non-genetic control over microbial phenotypes and complements genetic engineering approaches. It enables new possibilities for microbial design in biotechnology, medicine, and environmental applications where genetic modification is impractical or undesirable.

microbiology↗

Deep sea anaerobic microbial community couples the degradation of insoluble chitin to extracellular electron transfer

Chitin is a major structural component of arthropod exoskeletons, and an important carbon and nitrogen source in marine environments. In anoxic sediments, its degradation generates chitooligosaccharides and N-acetylglucosamine (GlcNAc), which are fermented into smaller organic molecules and oxidized anaerobically using soluble electron acceptors or insoluble ones such as metal oxides. To date, many aspects of chitin degradation in deep-sea anoxic sediments have been overlooked, including the potential coupling of insoluble chitin degradation to metal oxide reduction, the involvement of extracellular electron transfer (EET), and the spatial organization of the microorganisms involved. Using anoxic deep-sea sediments recovered from a whale fall site, we developed an innovative workflow based on electrochemical reactors, to characterize chitin degradation in these environments. Sediment samples enriched on poorly crystalline iron oxides, and subsequently transferred into an electrochemical reactor poised at +0.22 V vs SHE, showed active anodic current production when supplied with chitin, which increased 2-fold when amended with GlcNAc. Chitin reactors were dominated by Vallitalea (Firmicutes), Spirochaetota, Gammaproteobacteria and Desulfobacterota. Exoenzyme activity assays, metabolite profiling, and continued anodic current production confirmed ongoing chitin degradation linked to EET. We observed metabolic associations between chitin degraders and secondary consumers using in situ imaging (16S rRNA gene FISH coupled with BONCAT and nanoSIMS). These microbial partners, within the electrode-attached community, required close proximity to the poised electrode ([≤] 10 {micro}m) to remain metabolically active. Supporting these observations, cultured isolates of Vallitalea sp. and Trichloromonas sp. recovered from the whale fall site exhibited chitin degradation and electrochemical activity, respectively. When co-cultured in an bioelectrochemical reactor, the acetate produced by Vallitalea sp. during chitin degradation fueled Trichloromonas sp., which facilitated EET, hereby demonstrating that syntrophic interactions are used to couple anoxic chitin degradation to EET in deep-sea sediments. These findings exemplify the interspecies interactions and resource optimization occurring in hard-to-reach and largely unknown deep-sea ecosystems.

microbiology↗

1 Microbiome determinants of productivity in whiteleg shrimp aquaculture

Aquaculture holds immense promise for addressing the food needs of our growing global population. Yet, a quantitative understanding of the factors that control its efficiency and productivity has remained elusive. In this study, we address this knowledge gap by focusing on the microbiome determinants of productivity, more specifically animal survival and growth, for one of the most predominant animal species in global aquaculture, whiteleg shrimp (Penaeus vannamei). Through analysis of the shrimp-associated microbiome from 610 aquaculture samples across Asia and Latin America, we established the presence of core phylogenetic groups, widely prevalent across aquaculture conditions in disparate geographic locations and including both pathogenic and beneficial microbes. Focusing on early stages of growth (larval hatcheries), we showed that the composition of the microbiome alone can predict approximately 50% of the variation in shrimp larvae survival rates. Taxa associated with high survival rates share recently acquired genes that appear to be specific to aquaculture conditions. These genes are involved in the biosynthesis of growth factors and in protein degradation, underscoring the potential role of beneficial microorganisms in nutrient assimilation. In contrast, the predictability of the microbiome on the adult shrimp weight in grow-out farms is weaker (10-20%), akin to observations in the context of livestock. In conclusion, our study unveils a novel avenue for predicting productivity in shrimp aquaculture based on microbiome analysis. This paves the way for targeted manipulation of the microbiome as a strategic approach to enhancing aquaculture efficiency from the earliest developmental stages.

microbiology↗

The development of ecological systems along paths of least resistance

A long-standing question in biology is whether there are common principles that characterize the development of ecological systems (the appearance of a group of taxa), regardless of organismal diversity and environmental context. Classic ecological theory holds that these systems develop following a sequenced orderly process that generally proceeds from fast-growing to slow-growing taxa and depends on life-history trade-offs. However, it is also possible that this developmental order is simply the path with the least environmental resistance for survival of the component species and hence favored by probability alone. Here, we use theory and data to show that the order from fast-to slow-growing taxa is the most likely developmental path for diverse systems when local taxon interactions self-organize to minimize environmental resistance. First, we demonstrate theoretically that a sequenced development is more likely than a simultaneous one, at least until the number of iterations becomes so large as to be ecologically implausible. We then show that greater diversity of taxa and life histories improves the likelihood of a sequenced order from fast-to slow-growing taxa. Using data from bacterial and metazoan systems, we present empirical evidence that the developmental order of ecological systems moves along the paths of least environmental resistance. The capacity of simple principles to explain the trend in the developmental order of diverse ecological systems paves the way to an enhanced understanding of the collective features characterizing the diversity of life.

ecology↗

Linear-regression-based algorithms can succeed at identifying microbial functional groups despite the nonlinearity of ecological function

Microbial communities play key roles across diverse environments. Predicting their function and dynamics is a key goal of microbial ecology, but detailed microscopic descriptions of these systems can be prohibitively complex. One approach to deal with this complexity is to resort to coarser representations. Several approaches have sought to identify useful groupings of microbial species in a data-driven way. Of these, recent work has claimed some empirical success at de novo discovery of coarse representations predictive of a given function using methods as simple as a linear regression, against multiple groups of species or even a single such group (the EQO approach of Shan et al. [25]). This success seems puzzling, since modeling community function as a linear combination of contributions of individual species appears simplistic. However, the task of identifying a predictive coarsening of an ecosystem is distinct from the task of predicting the function well, and it is conceivable that the former could be accomplished by a simpler methodology than the latter. Here, we use the resource competition framework to design a model where the "correct" grouping to be discovered is well-defined, and use synthetic data to evaluate and compare three regression-based methods, namely, two proposed previously and one we introduce. We find that regression-based methods can recover the groupings even when the function is manifestly nonlinear; that multi-group methods offer an advantage over a single-group EQO; and crucially, that simpler (linear) methods can outperform more complex ones. Author summaryNatural microbial communities are highly complex, making predictive modeling difficult. One appealing approach is to make their description less detailed, rendering modeling more tractable while hopefully still retaining some predictive power. The Tree of Life naturally provides one possible method for building coarser descriptions (instead of thousands of strains, we could think about hundreds of species; or dozens of families). However, it is known that useful descriptions need not be taxonomically coherent, as illustrated, for example, by the so-called functional guilds. This prompted the development of computational methods seeking to propose candidate groupings in a data-driven manner. In this computational study, we examine one class of such methods, recently proposed in the microbial context. Quantitatively testing their performance can be difficult, as the answer they "should" recover is often unknown. Here, we overcome this difficulty by testing these methods on synthetic data from a model where the ground truth is known by construction. Curiously, we demonstrate that simpler approaches, rather than suffering from this simplicity, can in fact be more robust.

ecology↗

Widespread B-vitamin auxotrophy in marine particle-associated bacteria

Microbial community assembly is governed by trophic interactions that mediate the transfer of carbon sources and biomass building blocks between species. However, central metabolism corresponds to only a small fraction of the biosynthetic potential of microbes: metabolites such as antimicrobial compounds, signaling molecules, and co-factors are underexplored forces shaping microbial communities. Here, we focus on B vitamin exchange in coastal marine bacterial communities that degrade particulate organic matter and find that natural seawater communities are vitamin limited. While almost a third of bacterial isolates from these communities are B vitamin auxotrophs, the pioneering degraders that first arrive on particles are vitamin producers that likely support auxotrophs through cross-feeding. However, combining experiments and a resource-explicit model, we show that auxotroph growth is often not restored by coculture with vitamin producers, but rather requires lysis and subsequent vitamin recycling. Our results highlight the importance of vitamin auxotrophies and lysis-mediated cross-feeding as important factors controlling microbial community assembly and succession on marine particles.

microbiology↗

Targeted hypermutation of putative antigen sensors in multicellular bacteria

Diversity-generating retroelements (DGRs) are used by bacteria, archaea and viruses as a targeted mutagenesis tool. Through error-prone reverse transcription, DGRs introduce random mutations at specific genomic loci, enabling rapid evolution of these targeted genes. However, the function and benefits of DGR-diversified proteins in cellular hosts remains elusive. We find that 85% of DGRs from one of the major monophyletic lineages of DGR reverse transcriptases are encoded by multicellular bacteria, which often have two or more DGR loci in their genomes. Using the multicellular purple sulfur bacterium Thiohalocapsa sp. PB-PSB1 as an example, we characterized nine distinct DGR loci that cumulatively lead to more than 10294 possible different combinations of target polypeptides. With environmental metagenomes from individual Thiohalocapsa aggregates, we show that most of PB-PSB1s DGR targets are diversified across its biogeographic range, with spatial heterogeneity in the diversity of each locus. In PSB1 and other members of this lineage of cellular DGRs, diversified target genes are associated with NACHT-domain anti-phage defenses and putative ternary conflict systems previously shown to be enriched in multicellular bacteria. We propose that these DGR-diversified target genes act as antigen sensors that confer a form of adaptive immunity to their multicellular consortia. These findings have implications for the emergence of multicellularity, as the NACHT-domain anti-phage systems and ternary systems share both domain homology and conceptual similarities with the innate immune and programmed cell death pathways of plants and metazoans. SignificanceTo defend themselves against predators, bacteria employ a wide range of conflict systems, some of which are enriched in multicellular bacteria. Here, we show that numerous multicellular bacteria use related diversity-generating retroelements (DGRs) to diversify such conflict systems. Error-prone reverse transcription in DGRs introduces random, targeted mutations and rapid diversification. We used Thiohalocapsa PB-PSB1, a member of multicellular bacterial consortia, as a model to study this association between conflict systems and DGRs. We characterized the natural diversity of PB-PSB1 DGRs and propose they function as hypervariable antigen sensors. The accumulation of such DGR-diversified defense systems in multicellular bacteria emphasizes the fitness advantage of a rapidly diversifying immune system for the evolution of multicellularity.

microbiology↗

Mapping gut bacteria into functional niches reveals the ecological structure of human gut microbiomes

Microbiomes are an essential contributor to the metabolic activity in the human gastrointestinal tract. The fermentation of otherwise indigestible nutritional components like dietary fibers relies on a complex interplay of metabolic pathways that are distributed across the individual bacteria. Yet, which of the bacteria are responsible for which parts of the distributed metabolism and how they should be grouped together is insufficiently understood. Here, we present the NicheMap, an approach to map the different bacterial taxa that make up the gut microbiome onto the different functional niches of microbial carbohydrate fermentation. Our approach uses in vitro measurements of bacterial growth and metabolic activity to identify which bacterial taxa are responsible for which metabolic function in the relevant complex context of whole human fecal microbiomes. We identified characteristic taxa selected for by a panel growth substrates representative of dietary components that are resistant to digestion by host enzymes. These characteristic taxa offer predictions of which bacteria are stimulated by the various components of human diet. We validated these predictions using microbiome data from a human nutritional supplementation study. We suggest a template of how bacterial taxonomic diversity is organized along the trophic cascade of intestinal carbohydrate fermentation. We anticipate that our results and our approach will provide a key contribution towards building a structure-function map for gut microbiomes. Having such a map on hand is an important step in moving the microbiome from a descriptive science to an interventional one.

microbiology↗

Mutation-induced infections of phage-plasmids

Phage-plasmids are extra-chromosomal elements that act both as plasmids and as phages, whose eco-evolutionary dynamics remain poorly constrained. Here, we show segregational drift and loss- of-function mutations play key roles in the infection dynamics of a cosmopolitan phage-plasmid, allowing it to create continuous productive infections in a population of marine Roseobacter. Recurrent loss-of-function mutations in the phage repressor that controls prophage induction led to constitutively lytic phage-plasmids that spread rapidly throughout the population. The entire phage-plasmid genome was packaged into virions, which were horizontally transferred by re-infecting lysogenized cells, leading to an increase in phage-plasmid copy number and to a heterozygous phage repressor locus within re-infected cells. While wild-type repressor variants prevented induction of phage-plasmids in a cell, the uneven apportionment of phage-plasmids after cell division (i.e., segregational drift) led to the production of offspring carrying only the constitutively lytic phage-plasmid, thus restarting the lysis-reinfection-segregation life-cycle. Mathematical models and experiments showed that these dynamics lead to a continuous productive infection of the bacterial population in which lytic and lysogenic phage-plasmids coexist. An analysis of marine bacterial genomes shows that the same plasmid backbone here described carries different phages in the environment and disseminates trans-continentally, suggesting that the phage-plasmid strategy is relevant and widespread in nature. Together, our study describes how the interplay between phage infection and plasmid genetics provide a unique eco-evolutionary strategy for phage-plasmids.

microbiology↗

Annotation-free discovery of functional groups in microbial communities

Recent studies have shown that microbial communities are composed of groups of functionally cohesive taxa, whose abundance is more stable and better associated with metabolic fluxes than that of any individual taxon. However, identifying these functional groups in a manner that is independent from error-prone functional gene annotations remains a major open problem. Here, we develop a novel approach that identifies functional groups of taxa in an unsupervised manner, solely based on the patterns of statistical variation in species abundance and environmental parameters. We demonstrate the power of this approach on three distinct data sets. On data of replicate microcosm with heterotrophic soil bacteria, our unsupervised algorithm recovered experimentally validated functional groups that divide metabolic labor and remain stable despite large variation in species composition. When leveraged against the ocean microbiome data, our approach discovered a functional group that combines aerobic and anaerobic ammonia oxidizers, whose summed abundance tracks closely with nitrate concentrations in the water column. Finally, we show that our framework can enable the detection of species groups that are likely responsible for the production or consumption of metabolites abundant in animal gut microbiomes, serving as a hypothesis generating tool for mechanistic studies. Overall, this work advances our understanding of structure-function relationships in complex microbiomes and provides a powerful approach to discover functional groups in an objective and systematic manner.

ecology↗

Fundamental metabolic strategies of heterotrophic bacteria

Through their metabolism, heterotrophic microbes drive carbon cycling in many environments (1). These microbes consume (and produce) hundreds to thousands of different metabolic substrates, begging the question of what level of description is required to understand the metabolic processes structuring their communities: do we need to account for the detailed metabolic capabilities of each organism, or can these capabilities be understood in terms of a few well-conserved carbon utilization strategies that could be more easily interpreted and more robustly predicted? Based on the high-throughput phenotyping of a diverse collection of marine bacteria, we showed that the fundamental metabolic strategy of heterotrophic microbes can be understood in terms of a single axis of variation, representing their preference for either glycolytic (sugars) or gluconeogenic (amino and organic acids) carbon sources. Moreover, an organisms position on this axis is imprinted in its genome, allowing us to successfully predict metabolic strategy across the bacterial tree of life. Our analysis also unveils a novel and general association between metabolic strategy and genomic GC content, which we hypothesize results from the difference in C:N supply associated with typical sugar and acid substrates. Thus, our work reveals a fundamental constraint on microbial evolution that structures bacterial genomes and communities and can be leveraged to understand diversity in functional terms, beyond catalogs of genes and taxa.

microbiology↗

Chitin utilization by marine picocyanobacteria and the evolution of a planktonic lifestyle

Marine picocyanobacteria (Prochlorococcus and Synechococcus), the most abundant photosynthetic cells in the oceans, are generally thought to have a primarily single-celled and free-living lifestyle. However, we find that genes for breaking down chitin - an abundant source of organic carbon that primarily exists as particles - are widespread in this group. We further show that cells with a chitin degradation pathway display chitin degradation activity, attach to chitin particles and show enhanced growth under low light conditions when exposed to chitosan, a partially deacetylated form of chitin. Marine chitin is largely derived from arthropods, whose roots lie in the early Phanerozoic, 520-535 million years ago, close to when marine picocyanobacteria began colonizing the ocean. We postulate that attachment to chitin particles allowed benthic cyanobacteria to emulate their mat-based lifestyle in the water column, initiating their expansion into the open ocean, seeding the rise of modern marine ecosystems. Transitioning to a constitutive planktonic life without chitin associations along a major early branch within the Prochlorococcus tree led to cellular and genomic streamlining. Our work highlights how coevolution across trophic levels creates metabolic opportunities and drives biospheric expansions.

ecology↗

Intercellular collectivity is governed by enzyme secretion strategies in marine polysaccharide degrading bacteria

Polysaccharide breakdown by bacteria requires the activity of enzymes that degrade polymers extracellularly. This generates a localized pool of breakdown products that are accessible to the enzyme producers themselves as well as to other organisms. Marine bacterial taxa often show marked differences in the production and secretion of degradative enzymes that break down polysaccharides. These differences can have profound effects on the pool of diffusible breakdown products and hence on the ecological dynamics. However, the consequences of differences in enzymatic secretions on cellular growth dynamics and interactions are unclear. Here we combine experiments and models to study the growth dynamics of single cells within populations of marine Vibrionaceae strains that grow on the abundant marine polymer alginate, using microfluidics coupled to quantitative single-cell analysis and mathematical modelling. We find that strains that have low extracellular secretions of alginate lyases show stronger aggregative behaviors compared to strains that secrete high levels of enzymes. One plausible reason for this observation is that low secretors require a higher cellular density to achieve maximal growth rates in comparison with high secretors. Our findings indicate that increased aggregation increases intercellular synergy amongst cells of low-secreting strains. By mathematically modelling the impact of the level of degradative enzyme secretion on the rate of oligomer loss to diffusion, we find that enzymatic capability modulates the propensity of cells within clonal populations to cooperate or compete with each other. Our experiments and models demonstrate that marine bacteria display distinct aggregative behaviors and intercellular interactions based on their enzymatic secretion capabilities when growing on polysaccharides.

microbiology↗

A Genome-Scale Metabolic Model of Marine Heterotroph Vibrio splendidus sp. 1A01

While the Vibrio splendidus species is best known as an opportunistic pathogen in oysters, the Vibrio splendidus sp. 1A01 strain was first identified as an early colonizer of synthetic chitin particles incubated in seawater. To gain a better understanding of its metabolism, a genome-scale metabolic model (GSMM) of V. splendidus sp. 1A01 was reconstructed. GSMMs enable us to simulate all metabolic reactions in a bacterial cell using Flux Balance Analysis. A draft model was built using an automated pipeline from BioCyc. Manual curation was then performed based on experimental data, in part by gap-filling metabolic pathways and tailoring the models biomass reaction to V. splendidus sp. 1A01. The challenges of building a metabolic model for a marine microorganism like V. splendidus sp. 1A01 are described.

microbiology↗

Turnover in life strategies recapitulates microbial succession on synthetic marine particles

Particulate organic matter (POM) in the ocean sustains diverse communities of bacteria that mediate the remineralization of organic complex matter. However, the variability of these particles and of the environmental conditions surrounding them present a challenge to the study of the ecological processes shaping particle-associated communities and their function. In this work, we utilise data from experiments in which coastal water communities were grown on synthetic particles to ask which are the most important ecological drivers of their assembly and associated traits. Combining 16S rRNA amplicon sequencing with shotgun metagenomics, together with an analysis of the full genomes of a subset of isolated strains, we were able to identify two-to-three distinct community classes, corresponding to early vs. late colonizers. We show that these classes are shaped by environmental selection (early colonizers) and facilitation (late colonizers), and find distinctive traits associated with each class. While early colonizers have a larger proportion of genes related to uptake of nutrients, motility and environmental sensing with few pathways enriched for metabolism, late colonizers devote a higher proportion of genes for metabolism, comprising a wide array of different pathways including metabolism of carbohydrates, amino acids and xenobiotics We find evidence in selected metabolic pathways for the existence of a trophic-chain topology connecting both classes. The interpretation of these traits suggests a distinction between early and late colonizers analogous to other classifications found in the literature, and we discuss connections with the classical distinction between r- and K-strategists.

microbiology↗

Bacterial growth in multicellular aggregates leads to the emergence of complex lifecycles

In response to environmental stresses such as starvation, many bacteria facultatively aggregate into multicellular structures that can attain new metabolic functions and behaviors. Despite the ubiquity and relevance of this form of collective behavior, we lack an understanding of how the spatiotemporal dynamics of aggregate development emerge from cellular physiology. Here, we show that the coupling between growth and spatial gradient formation leads to the emergence of a complex lifecycle, akin to those known for multicellular bacteria. Under otherwise carbon-limited growth conditions, the marine bacterium Vibrio splendidus 12B01 forms multicellular groups to collectively harvest carbon from the brown-algal polysaccharide alginate. This is achieved during growth on dissolved alginate polymer through formation of spherical, clonal clusters of cells that grow up to 40 {micro}m in radius. Clusters develop striking spatial patterning as they grow due to phenotypic differentiation of sub-populations into a shell of static cells surrounding a motile core. Combining in situ measurements of cell physiology with transcriptomics, we show that shell cells express adhesive type IV pili, while motile core cells express carbon storage granules. The emergence of shell and core phenotypes is cued by opposing gradients of carbon and nitrogen that form within cell clusters due to local metabolic activity. Eventually, the shell ruptures, releasing the carbon-storing core, and we show that carbon-storing cells more readily propagate on alginate than non-carbon storing cells. We propose that phenotypic differentiation promotes the resilience of 12B01 groups by enabling clonal groups to grow larger and propagate more effectively. Phenotypic differentiation may be a widespread, but overlooked, strategy among bacteria to enhance resilience in the context of resource limitation.

microbiology↗

Viral infection switches the balance between bacterial and eukaryotic recyclers of organic matter during algal blooms

Algal blooms are hotspots of marine primary production and play central roles in microbial ecology and global nutrient cycling. When blooms collapse, organic carbon is transferred to higher trophic levels, microbial respiration or sinking in proportions that depend on the dominant mortality agent. Viral infection can lead to bloom termination, but its impact on the fate of carbon remains an open question. Here, we characterized the consequences of viral infection on the microbiome composition and biogeochemical landscape of marine ecosystems by conducting a large-scale mesocosm experiment. Moniroting of seven induced coccolithophore blooms, which showed different degrees of viral infection, revealed that only high levels of viral infection caused significant shifts in the composition of free-living bacterial and eukaryotic assemblages. Intriguingly, viral infection favored the growth of eukaryotic heterotrophs (thraustochytrids) over bacteria as potential recyclers of organic matter. By combining modeling and quantification of active viral infection at a single-cell resolution, we estimate that viral infection can increase per-cell rates of extracellular carbon release by 2-4.5 fold. This happened via production of acidic polysaccharides and particulate inorganic carbon, two major contributors to carbon sinking into the deep ocean. These results reveal the impact of viral infection on the fate of carbon through microbial recyclers of organic matter in large-scale coccolithophore blooms.

microbiology↗