Evolutionary ecology of human-associated microbes

Determining the evolutionary mechanisms, genomic outcomes and functional consequences of adaptation is of paramount importance for our understanding of the nature of evolution, and for predicting the evolutionary responses of organisms in the face of the current and future global changes. Microorganisms which are associated with humans (as members of the human microbiome, or associated with domesticated plants or animals) provide ideal models to study adaptation and specialisation. These microbes are diverse and many possess outstanding experimental assets, such as small genomes and membership in relatively simple multi-species communities (Gladieux et al., 2014; Rosshart et al., 2019; Seybold et al., 2020). In addition, studying microbial evolution in human-associated environments is effective because population genetic processes (i.e. genetic drift and selection) are often strong and recent (Gladieux et al., 2014; Ropars & Giraud, 2022). Furthermore, human-associated microbes often have important impacts on human health as members of our microbiomes, as human pathogens or as associates of food production for crop microbiomes, crop pathogens and domesticated microorganisms (Caron et al., 2021; Chow et al., 2020; Davenport et al., 2017; Fisher et al., 2020; Seybold et al., 2020; Wolfe et al., 2014). This special issue covers a broad range of topics related to the evolutionary ecology of human-associated microbes, with methods ranging from population genetics to metagenomics and evolutionary genomics, as well as complementary field and lab studies (in vitro and in vivo). The study organisms include domesticated microorganisms (fungi and bacteria), microorganisms thriving in anthropic environments, host-associated microbiota, crop pathogens and animal pathogens. Together these articles underline the huge impact of the anthropogenic environment in microbial evolution, including the emergence and spread of pathogens as well as the benefits provided by domesticated or mutualistic fungi and bacteria. The yeast Brettanomyces bruxellensis has adapted to many different anthropic environments, for example, wine, beer, bioethanol production and kombucha. While it can be desired and used as a starter for adding a spicy phenolic note to some beer types, it can also be considered as a spoiler, as it causes unpleasant aromas in wine (e.g. barnyard, horse swear or burnt plastic-like aromas) and a reduction of ethanol yield in bioethanol production. In their review, Harrouard et al. (2023) describe the genetic and phenotypic diversity of this yeast, highlighting the role of polyploidisation and hybridisation as one of the driving mechanisms for the adaptation of B. bruxellensis to various anthropic niches. Some populations of B. bruxellensis may even be considered as domesticated, as beer strains have acquired the ability to metabolise maltose and to produce pleasant aromas. Conversely, other populations are notorious spoilers, such as those producing unpleasant aromas in wine. These populations have adapted to the human-made beverage, having acquired tolerance or resistance against the sulphite added to control endemic non-Saccharomyces yeasts, including B. bruxellensis. Other yeasts have been genuinely domesticated, that is, have evolved specific traits under selection by humans for making better foods or drinks. Genetic differentiation in domesticated yeasts is often driven by geography and ecological niche, as found in B. bruxellensis, S. cerevisiae and Torulaspora delbrueckii (Silva et al., 2023). This latter yeast is associated with winemaking, bread, dairy products and also with natural environments such as soil or plants. The population genomic analyses by Silva et al. (2023) revealed the acquisition of a cluster of GAL genes, associated with galactose metabolism, only in dairy strains, and the expansion and functional diversification of MAL genes associated with maltose metabolism in bread dough strains. This likely represents a genomic footprint of domestication. Fermented products are most often formed by microbial communities (including bacteria, yeasts and sometimes moulds), and not only by inoculated microorganisms. Identifying the origins of microorganisms in such communities is often challenging. von Gastrow et al. (2023) studied the microbial communities in sourdough, a naturally fermented mixture of flour and water for making bread. They used a combination of lab experiments, metabarcoding and participatory research approaches to understand the origin of the microorganisms in sourdough. The core microbiota detected on the seeds and in the flour were mainly composed of microbes known to be associated with plants and were absent in sourdoughs. Conversely, no sourdough yeast species were detected on grains and flours, leaving the origin of sourdough yeasts unresolved. Invasions by fungal plant pathogens represent a significant threat to crop production. Population genome sequencing in Colletotrichum truncatum, an invasive pathogen on soybean in Brazil, revealed three distinct lineages that hybridise one with each other (Rogério et al., 2023); the introgressions involved in particular secreted protein-encoding genes, and may therefore be under selection for host infection (Rogério et al., 2023). Gene flow can indeed foster rapid adaptation. Gene copy-number variation is another type of genomic feature under selection within and between populations. Using comparative genomics and genome wide association, Stalder et al. (2023) found that copy number variants in Rhynchosporium commune, a major pathogen of barley, are enriched in genes related to host exploitation and fungicide resistance. The authors further showed that gene copy-number variation was most often associated with segmental duplication near recently active transposable elements, thus adding to the growing evidence of mobile genetic elements being important players in generating genome variation with adaptive potential. To fight crop pathogens, Saubin et al. (2023) argue that we should bridge gaps between separated fields, in particular between plant breeding, the study of molecular interactions and epidemiology and evolution. This could be achieved using the theoretical framework of population genetics and would provide an integrated view of pathogen adaptation, allowing to optimally manage genetically resistant cultivars. Growing plant varieties carrying resistance genes (R) on large scales in landscapes indeed induces a strong selection on pathogen populations, leading to the rapid evolution of new virulence abilities. This occurred in the poplar rust fungus Melampsora larici-populina with the breakdown of the poplar RMlp7 resistance gene. An unprecedented monitoring across 28 years of the variation at the candidate avirulence gene AvrMlp7 revealed that two avirulent alleles, corresponding to a nonsynonymous mutation and a complete deletion of the locus, occurred before the resistance breakdown event (Louet et al., 2023). This case study therefore represents a major adaptive event from standing variation. Population genetics predicts that diseases should be less frequent in populations of hosts with higher levels of genetic diversity. Genotyping-by-sequencing in Arabica coffee sites in southwestern Ethiopia showed that genetic diversity in coffee trees was higher in less managed sites and the incidence of four major fungal diseases was related to the genetic composition of the coffee stands (Zewdie et al., 2023). Genetic diversity in coffee trees was also related to the within-site variation of coffee berry disease, but not to the mean incidence of any of the four studied diseases across sites (Zewdie et al., 2023). Wang et al. (2023) explored the diversity of pathogenic fungi infecting wheat heads, and belonging to the genus Fusarium. They characterised the diversity of Fusarium species in wheat heads across different geographical regions in China and simultaneously recorded the diversity of mycotoxins produced by these fungi. Mycotoxins are secondary metabolites produced by Fusarium that reduce grain quality. The study demonstrates a high species diversity of Fusarium on wheat heads, and moreover shows how this diversity has relevance for the accumulation and diversity of mycotoxins. Interestingly, the diversity of Fusarium species is negatively correlated with mycotoxin accumulation, as elegantly demonstrated in an experiment where single and multi-species Fusarium spore suspensions are inoculated onto wheat heads. The study points to the importance of microbe-microbe interactions in shaping disease development and fungal metabolite production, an observation of great relevance in the context of disease treatment and crop protection. Traditional agrosystems in which disease outbreaks are rare can also help identify sustainable agricultural practices. Genomic and phenotypic analyses of paired samples of rice landraces and strains of the rice blast fungal pathogen (Pyricularia oryzae) in the traditional Yuanyang terraces of flooded rice paddies in China revealed high levels of genetic diversity and a generalist life history in the pathogen (Ali et al., 2023). The traditional agricultural practices with high plant genetic diversity thus likely favoured generalist strategies in the pathogen, which overall reduces the burden of disease. Together, population genetic and genomic studies of pathogens associated with crops demonstrate the exceptional speed whereby pathogens can disperse and adapt. Rapid evolution of pathogens associated with agricultural crops is fuelled by the uniform composition of agricultural monoculture fields. Eco-evolutionary dynamics of microbial communities are strongly impacted by human activities. These interactions can operate on multiple scales. On a broad scale, human activities can cause spatial variation in environments. As a result, humans themselves are exposed to different environments across space and time, and animals in habitats that are close to human settlements may also be exposed to different environments. Yuan et al. (2023) and Pedro et al. (2023) examine how these patterns of spatial environmental variation can affect the microbiome. Yuan et al. (2023) show that human impacts on the habitats of roe deer in China lead to different roe deer diets. These diets are associated with different gut microbiota that appear to be better suited to help the deer process those diets. Similarly, Pedro et al. (2023) show that the human oral microbiome shows geographical patterns in Papua New Guinea. These patterns may be linked to diet/ecology, ancestry, and/or lifestyle. Microbial interactions have a great impact on disease development in humans and animals. MacAlpine et al. (2023) review current literature focused on interactions of bacteria and fungi that colonise humans. Candida albicans, Cryptococcus neoformans, and Aspergillus fumigatus are three fungal species which are responsible for most systemic infections in humans. As these fungi colonise different niches of the human body they interact with diverse bacterial communities. Several studies have identified the importance of fungal–bacterial interactions during colonisation and disease development of skin, lungs and the intestinal tract. The nature of these diverse interactions are still poorly understood, however, research into microbial interactions holds a great potential for the discovery of new antimicrobial and antifungal compounds. On a smaller scale, it is also clear that human daily practices can affect microbial communities. Multiple studies in this special issue examine dynamics at this scale, testing between different processes of host–microbe interactions and microbial community assembly while integrating information about specific human behaviours and their impact. Moeller (2023) examines the human gut microbiota using a population approach and finds that antibiotics drive balancing selection in the gut microbiota. This process maintains allelic diversity implicated in drug resistance and is most apparent in industrialised populations. Similarly, Tessandier et al. (2023) test the effect of different types of menstruation protection on the vaginal microbiota. Although they do not find strong patterns, some clustering suggests that different types of protection could lead to vaginal changes that affect the microbiota. Peimbert and Alcaraz (2023) consider human commuter behaviour, reviewing the existing literature on the subway microbiome. They link data describing the built environment and the skin microbiota and emphasise the need for more information about specific human behaviours in the subway (sit/hold/etc., cleaning routine of subways, etc.) and how they affect microbial communities. They also highlight the need for understanding which microbes are pathogenic or not and alive or not to determine health implications. Finally, Bischofberger and Hall (2023) consider human economic behaviour in the context of banknotes and money exchange. They demonstrate that niche-based processes such as local habitat more strongly influence the microbial community of Swiss banknotes than dispersal-based processes like geographic distance. Given that the local habitat of banknotes is affected by human shopping behaviour, and that everyday contact with banknotes could also affect the human microbiota, this study provides an interesting new perspective for considering eco-evolutionary dynamics in the human microbiome. Corsi et al. (2023) address the origin of new human diseases by focusing on the zoonotic parasite Cryptosporidium parvum. This parasite belongs to the phylum Apicomplexa which also includes the Malaria parasite Plasmodium falciparum. In their study, Corsi et al. (2023) analyse the genomic diversity of C. parvum obtained from human and ruminants collected across Europe, Egypt and China. They demonstrate recent recombination between human and animal infecting lineages and suggest that recombination across host-boundaries may be an important source of new genetic variation and rapid adaptation of such zoonotic pathogens. The recent Covid-19 pandemic exemplifies the importance of studying pathogens associated with animals in human environments. Inasmuch studying human-associated microbes can shed light on general evolutionary processes, the study of wild populations sets the reference to which human influence on these processes needs to be evaluated. Sinorhizobium meliloti (a.k.a. Ensifer meliloti) is a nitrogen-fixing bacteria closely related to symbionts of major legume crops such as soybean, alfalfa and peanut. Studying the population structure of bacterial chromosomes and mobile genetic elements of S. meliloti strains sampled across South Western Europe, Riley et al. (2023) found that within-site variation is more important than between-site variation and that the three genetic elements have distinct population structures, all three being discordant with the population structure of their natural host (Medicago truncatula). Authors also showed that recombination rates of mobile genetic elements are at least one order of magnitude greater than those of the chromosome. Strong population structure in the host and lack thereof in the symbionts suggest that different host populations interact with genetically similar symbionts, thus hampering local adaptation. Whether this is the case for crop legume hosts and their symbionts remains to be established. Richard et al. (2023) provide further evidence for the relevance of gene transfer among bacterial taxa. In their study they have focused on plasmid-encoding genes in the bacterial family Lysobacteraceae which includes important plant pathogenic bacteria and opportunistic human pathogens. Plasmids of Lysobacteraceae carry genes conferring functions related to pathogenicity and microbe-microbe interactions. These genes appear to be highly dynamic and readily exchanged across species boundaries. Interestingly, the authors find that different bacterial lifestyles constitute barriers to gene transfer although transfers can occur between very distantly related bacteria. This observation highlights the potential for rapid evolution of bacteria associated with human and agricultural environments and demonstrates that gene transfer is a mechanism to facilitate the fast establishment of bacteria into new niches. Mycorrhizal fungi is another group of plant mutualists. Arbuscular mycorrhizal fungi form symbiosis with plant roots and provide their host with nutrients, primarily phosphorus. Understanding the diversity and stability of mycorrhizal communities in agricultural soils is of great importance to predict how environmental change will impact beneficial symbioses in plant roots. Gao et al. (2023) have investigated the consequences of drought stress on mycorrhizal diversity using a large-scale field experiment of sorghum. Hereby they profiled the succession of microbial diversity associated with sorghum roots focusing specifically on mycorrhizal diversity. As predicted, mycorrhizal communities change in response to plant stress, however the change does not correspond to a replacement of competitive mycorrhizal species with non-competitive species (ruderal). Rather the change correlates with altered expression of plant genes which may play a role in regulating mycorrhiza symbiosis. To which extent mycorrhizal succession correlates with plant selection for optimal symbiotic partners is yet to be determined. However, the study underlines the necessity of understanding the impact of environmental changes and abiotic stresses on the diversity and function of plant-associated microbes. Over thousands of years, human activities have enormously changed ecosystems across the planet. Hereby we have also impacted the diversity and function of microbes associated with domesticated plants and animals. Advances in sequencing techniques have provided new tools to characterise microbial diversity from the level of individual populations to communities. Studies focused on pathogenic species associated with crops and husbandry have demonstrated the great impact of agriculture on microbial diversity and evolution. The uniform architecture of agricultural systems not only favours the rapid evolution and dispersal of pathogens but also promotes host jumps between crop species and between animal husbandry and humans. The application of antimicrobials and antifungals have, in the past decades, been an important solution to combat pathogens in medical as well as agricultural contexts. However, the usage of such compounds have multiple downsides; first of all they also target non-pathogenic microbes and thereby alter native microbiomes. Moreover, continuous usage of antimicrobials selects for microbial resistance and thereby the loss of compound efficacy. Resistance mutations may rapidly spread in an environment where resistance is advantageous, and the spread can occur within populations as well as across species boundaries by horizontal gene transfer. This special issue presents new research of evolutionary processes in microbes associated with our near environment including human-associated microbes and microbes associated with food production. Understanding the evolutionary ecology of these microbes is of critical importance for future applications intended to promote beneficial microbial symbionts and to control pathogens.