Understanding the principles that govern the assembly of microbial communities across earth's biomes is a major challenge in modern microbial ecology. This pursuit is complicated by the difficulties of mapping functional roles and interactions onto communities with immense taxonomic diversity and of identifying the scale at which microbes interact [1]. To address this challenge, here, we focused on the bacterial communities that colonize and degrade particulate organic matter in the ocean [2-4]. We show that the assembly of these communities can be simplified as a linear combination of functional modules. Using synthetic polysaccharide particles immersed in natural bacterioplankton assemblages [1, 5], we showed that successional particle colonization dynamics are driven by the interaction of two types of modules: a first type made of narrowly specialized primary degraders, whose dynamics are controlled by particle polysaccharide composition, and a second type containing substrate-independent taxa whose dynamics are controlled by interspecific interactions-in particular, cross-feeding via organic acids, amino acids, and other metabolic byproducts. We show that, as a consequence of this trophic structure, communities can assemble modularly-i.e., by a simple sum of substrate-specific primary degrader modules, one for each complex polysaccharide in the particle, connected to a single broad-niche range consumer module. Consistent with this model, a linear combination of the communities on single-polysaccharide particles accurately predicts community composition on mixed-polysaccharide particles. Our results suggest that the assembly of heterotrophic communities that degrade complex organic materials follows simple design principles that could be exploited to engineer heterotrophic microbiomes.

In spite of its major impact on life-long health, the process of microbial succession in the gut of infants remains poorly understood. Here, we analyze the patterns of taxonomic and functional change in the gut microbiota during the first year of life for a birth cohort of 13 infants. We detect that individual instances of gut colonization vary in the temporal dynamics of microbiota richness, diversity, and composition at both functional and taxonomic levels. Nevertheless, trends discernible in a majority of infants indicate that gut colonization occurs in two distinct phases of succession, separated by the introduction of solid foods to the diet. This change in resource availability causes a sharp decrease in the taxonomic richness of the microbiota due to the loss of rare taxa (p = 2.06e-9), although the number of core genera shared by all infants increases substantially. Moreover, although the gut microbial succession is not strictly deterministic, we detect an overarching directionality of change through time towards the taxonomic and functional composition of the maternal microbiota. Succession is however not complete by the one year mark, as significant differences remain between one-year-olds and their mothers in terms of taxonomic (p = 0.009) and functional (p = 0.004) microbiota composition, and in taxonomic richness (p = 2.76e-37) and diversity (p = 0.016). Our results also indicate that the taxonomic composition of the microbiota shapes its functional capacities. Therefore, the observed inter-individual variability in taxonomic composition during succession is not fully compensated by functional equivalence among bacterial genera and may have important physiological consequences. Finally, network analyses suggest that positive interactions among core genera during community assembly contribute to ensure their permanence within the gut, and highlight an expansion of complexity in the interactions network as the core of taxa shared by all infants grows following the introduction of solid foods. Although knowledge of the complex community of microbes that inhabits the human gut is constantly increasing, the successional process through which it develops during infancy remains poorly understood. Particularly, although gut microbiota composition is known to vary through time among infants, the effect of this variability on the functional capacities of the community has not been previously explored. We simultaneously analyze the taxonomic and functional development of the gut microbiota in a birth cohort of healthy infants during the first year of life, showing that individual instances of gut colonization vary in their temporal dynamics and that clear parallelisms exist between functional and taxonomic change. Therefore, taxonomic composition shapes the functional capacities of the microbiota, and, consequently, successional variability may affect host physiology, metabolism and immunity. Nevertheless, we detect some overarching trends in microbiota development, such as the existence of two distinct phases of succession, separated by the introduction of solid foods, and a strong directionality of change towards the taxonomic and functional composition of the maternal microbiota. Understanding the commonalities and differences among individual patterns of gut colonization in healthy infants will enable a better definition of the deviations in this process that result in microbiota imbalances and disease.

Recent theory and experiments have reported a reproducible tendency for the coexistence of microbial species under controlled environmental conditions. This observation has been explained in the context of competition for resources and metabolic complementarity given that, in microbial communities (MCs), many excreted by-products of metabolism may also be resources. MCs therefore play a key role in promoting their own stability and in shaping the niches of the constituent taxa. We suggest that an intermediate level of organization between the species and the community level may be pervasive, where tightly knit metabolic interactions create discrete consortia that are stably maintained. We call these units Metabolically Cohesive Consortia (MeCoCos) and we discuss the environmental context in which we expect their formation, and the ecological and evolutionary consequences of their existence. We argue that the ability to identify MeCoCos would open new avenues to link the species-, community- and ecosystem-level properties, with consequences for our understanding of microbial ecology and evolution, and an improved ability to predict ecosystem functioning in the wild. This article is part of the theme issue ‘Conceptual challenges in microbial community ecology’.

A key question of theoretical ecology is which properties of ecosystems favour their stability and help maintaining biodiversity. This question recently reconsidered mutualistic systems, generating intense controversy about the role of mutualistic interactions and their network architecture. Here we show analytically and verify with simulations that reducing the effective interspecific competition and the propagation of perturbations positively influences structural stability against environmental perturbations, enhancing persistence. Noteworthy, mutualism reduces the effective interspecific competition only when the direct interspecific competition is weaker than a critical value. This critical competition is in almost all cases larger in pollinator networks than in random networks with the same connectance. Highly connected mutualistic networks reduce the propagation of environmental perturbations, a mechanism reminiscent of MacArthur’s proposal that ecosystem complexity enhances stability. Our analytic framework rationalizes previous contradictory results, and it gives valuable insight on the complex relationship between mutualism and biodiversity.

A central goal in microbial ecology is to simplify the extraordinary biodiversity that inhabits natural environments into ecologically coherent units. We profiled (16S rRNA sequencing) > 700 semi-aquatic bacterial communities while measuring their functional capacity when grown in laboratory conditions. This approach allowed us to investigate the relationship between composition and function excluding confounding environmental factors. Simulated data allowed us to reject the hypothesis that stochastic processes were responsible for community assembly, suggesting that niche effects prevailed. Consistent with this idea we identified six distinct community classes that contained samples collected from distant locations. Structural equation models showed there was a functional signature associated with each community class. We obtained a more mechanistic understanding of the classes using metagenomic predictions (PiCRUST). This approach allowed us to show that the classes contained distinct genetic repertoires reflecting community-level ecological strategies. The ecological strategies resemble the classical distinction between r- and K-strategists, suggesting that bacterial community assembly may be explained by simple ecological mechanisms.