Leaf‐cutter ants are a prominent feature in Neotropical ecosystems, but a comprehensive assessment of their effects on ecosystem functions is lacking. We reviewed the literature and used our own recent findings to identify knowledge gaps and develop a framework to quantify the effects of leaf‐cutter ants on ecosystem processes. Leaf‐cutter ants disturb the soil structure during nest excavation changing soil aeration and temperature. They mix relatively nutrient‐poor soil from deeper layers with the upper organic‐rich layers increasing the heterogeneity of carbon and nutrients within nest soils. Leaf‐cutter ants account for about 25% of all herbivory in Neotropical forest ecosystems, moving 10%–15% of leaves in their foraging range to their nests. Fungal symbionts transform the fresh, nutrient‐rich vegetative material to produce hyphal nodules to feed the ants. Organic material from roots and arbuscular mycorrhizal fungi enhances carbon and nutrient turnover in nest soils and creates biogeochemical hot spots. Breakdown of organic matter, microbial and ant respiration, and nest waste material decomposition result in increased CO2, CH4, and N2O production, but the build‐up of gases and heat within the nest is mitigated by the tunnel network ventilation system. Nest ventilation dynamics are challenging to measure without bias, and improved sensor systems would likely solve this problem. Canopy gaps above leaf‐cutter ant nests change the light, wind and temperature regimes, which affects ecosystem processes. Nests differ in density and size depending on colony age, forest type and disturbance level and change over time resulting in spatial and temporal changes of ecosystem processes. These characteristics remain a challenge to evaluate rapidly and non‐destructively. Addressing the knowledge gaps identified in this synthesis will bring insights into physical and biological processes driving biogeochemical cycles at the nest and ecosystem scale and will improve our understanding of ecosystem biogeochemical heterogeneity and larger scale ecological phenomena. A plain language summary is available for this article.

The evolutionary success of hymenopteran insects has been associated with complex physiological and behavioral defense mechanisms against pathogens and parasites. Among these strategies are symbiotic associations between Hymenoptera and antibiotic-producing Actinobacteria, which provide protection to insect hosts. Herein, we examine associations between culturable Actinobacteria and 29 species of tropical hymenopteran insects that span five families, including Apidae (bees), Vespidae (wasps), and Formicidae (ants). In total, 197 Actinobacteria isolates were obtained from 22 of the 29 different insect species sampled. Through 16S rRNA gene sequences of 161 isolates, we show that 91% of the symbionts correspond to members of the genus Streptomyces with less common isolates belonging to Pseudonocardia and Amycolatopsis. Electron microscopy revealed the presence of filamentous bacteria with Streptomyces morphology in brood chambers of two different species of the eusocial wasps. Four fungal strains in the family Ophiocordycipitacea (Hypocreales) known to be specialized insect parasites were also isolated. Bioassay challenges between the Actinobacteria and their possible targeted pathogenic antagonist (both obtained from the same insect at the genus or species level) provide evidence that different Actinobacteria isolates produced antifungal activity, supporting the hypothesis of a defensive association between the insects and these microbe species. Finally, phylogenetic analysis of 16S rRNA and gyrB demonstrate the presence of five Streptomyces lineages associated with a broad range of insect species. Particularly our Clade I is of much interest as it is composed of one 16S rRNA phylotype repeatedly isolated from different insect groups in our sample. This phylotype corresponds to a previously described lineage of host-associated Streptomyces. These results suggest Streptomyces Clade I is a Hymenoptera host-associated lineage spanning several new insect taxa and ranging from the American temperate to the Neotropical region. Our work thus provides important insights into the widespread distribution of Actinobacteria and hymenopteran insects associations, while also pointing at novel resources that could be targeted for the discovery of active natural products with great potential in medical and biotechnological applications.

Examining the population structure and the influence of recombination and ecology on microbial populations makes great sense for understanding microbial evolution and speciation. Streptomycetes are a diverse group of bacteria that are widely distributed in nature and a rich source of useful bioactive compounds; however, they are rarely subjected to population genetic investigations. In this study, we applied a five-gene-based multilocus sequence analysis (MLSA) scheme to 41 strains of Streptomyces albidoflavus derived from diverse sources, mainly insects, sea, and soil. Frequent recombination was detected in S. albidoflavus, supported by multiple lines of evidence from the pairwise homoplasy index (⌽ w ) test, phylogenetic discordance, the Shimodaira-Hasegawa (SH) test, and network analysis, underpinning the predominance of homologous recombination within Streptomyces species. A strong habitat signal was also observed in both phylogenetic and Structure 2.3.3 analyses, indicating the importance of ecological difference in shaping the population structure. Moreover, all three habitat-associated groups, particularly the entomic group, demonstrated significantly reduced levels of gene flow with one another, generally revealing habitat barriers to recombination. Therefore, a combined effect of homologous recombination and ecology is inferred for S. albidoflavus, where dynamic evolution is at least partly balanced by the extent that differential distributions of strains among habitats limit genetic exchange. Our study stresses the significance of ecology in microbial speciation and reveals the coexistence of homologous recombination and ecological divergence in the evolution of streptomycetes. Despite various currently available approaches to defining prokaryotic species and a growing recognition of their vast diversity in nature, the concept of microbial species has long been under dispute due to their widespread genomic heterogeneity and variable levels of gene exchange (1-3). Genetic clusters that emerge in molecular sequence analyses of populations are often regarded as bearing the status of species, and multiple theoretical models to resolve the evolutionary mechanisms that cause the creation and maintenance of the genetic clusters have been proposed (3, 4). Until now, two major parallel concepts of microbial species have been developed, focused on barriers to recombination and ecological divergence, respectively (4): the neutral model, raised by Fraser and colleagues (3, 5), highlights the role of recombination in converging and diverging clusters with various recombination rates, while the ecotype model, developed by Cohan and colleagues (6, 7), defines an ecotype as a group of ecologically similar strains which is purged of its diversity by periodic selection and/or genetic drift. Consequently, recombination and divergent selection have emerged as two key processes driving the increasing discussion concerning theoretical models of microbial speciation. Moreover, coexistence of these processes has been suggeste...

Despite advances in sequencing, lack of standardization makes comparisons across studies challenging and hampers insights into the structure and function of microbial communities across multiple habitats on a planetary scale. Here we present a multi-omics analysis of a diverse set of 880 microbial community samples collected for the Earth Microbiome Project. We include amplicon (16S, 18S, ITS) and shotgun metagenomic sequence data, and untargeted metabolomics data (liquid chromatography-tandem mass spectrometry and gas chromatography mass spectrometry). We used standardized protocols and analytical methods to characterize microbial communities, focusing on relationships and co-occurrences of microbially related metabolites and microbial taxa across environments, thus allowing us to explore diversity at extraordinary scale. In addition to a reference database for metagenomic and metabolomic data, we provide a framework for incorporating additional studies, enabling the expansion of existing knowledge in the form of an evolving community resource. We demonstrate the utility of this database by testing the hypothesis that every microbe and metabolite is everywhere but the environment selects. Our results show that metabolite diversity exhibits turnover and nestedness related to both microbial communities and the environment, whereas the relative abundances of microbially related metabolites vary and co-occur with specific microbial consortia in a habitat-specific manner. We additionally show the power of certain chemistry, in particular terpenoids, in distinguishing Earth’s environments (for example, terrestrial plant surfaces and soils, freshwater and marine animal stool), as well as that of certain microbes including Conexibacter woesei (terrestrial soils), Haloquadratum walsbyi (marine deposits) and Pantoea dispersa (terrestrial plant detritus). This Resource provides insight into the taxa and metabolites within microbial communities from diverse habitats across Earth, informing both microbial and chemical ecology, and provides a foundation and methods for multi-omics microbiome studies of hosts and the environment.

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