A growing world population and an increasing demand for greater food production requires that crop losses caused by pests and diseases are dramatically reduced. Concurrently, sustainability targets mean that alternatives to chemical pesticides are becoming increasingly desirable. Bacteria in the plant root microbiome can protect their plant host against pests and pathogenic infection. In particular, Streptomyces species are well-known to produce a range of secondary metabolites that can inhibit the growth of phytopathogens. Streptomyces are abundant in soils and are also enriched in the root microbiomes of many different plant species, including those grown as economically and nutritionally valuable cereal crops. In this review we discuss the potential of Streptomyces to protect against some of the most damaging cereal crop diseases, particularly those caused by fungal pathogens. We also explore factors that may improve the efficacy of these strains as biocontrol agents in situ, as well as the possibility of exploiting plant mechanisms, such as root exudation, that enable the recruitment of microbial species from the soil to the root microbiome. We argue that a greater understanding of these mechanisms may enable the development of protective plant root microbiomes with a greater abundance of beneficial bacteria, such as Streptomyces species.
Acromyrmex leafcutter ants form a mutually beneficial symbiosis with the fungus Leucoagaricus gongylophorus and with Pseudonocardia bacteria. Both are vertically transmitted and actively maintained by the ants. The fungus garden is manured with freshly cut leaves and provides the sole food for the ant larvae, while Pseudonocardia cultures are reared on the ant-cuticle and make antifungal metabolites to help protect the cultivar against disease. If left unchecked, specialized parasitic Escovopsis fungi can overrun the fungus garden and lead to colony collapse. We report that Escovopsis upregulates the production of two specialized metabolites when it infects the cultivar. These compounds inhibit Pseudonocardia and one, shearinine D, also reduces worker behavioral defenses and is ultimately lethal when it accumulates in ant tissues. Our results are consistent with an active evolutionary arms race between Pseudonocardia and Escovopsis, which modifies both bacterial and behavioral defenses such that colony collapse is unavoidable once Escovopsis infections escalate.
Background: The vertebrate gut microbiome (GM) can vary substantially across individuals within the same natural population. Although there is evidence linking the GM to health in captive animals, very little is known about the consequences of GM variation for host fitness in the wild. Here, we explore the relationship between faecal microbiome diversity, body condition, and survival using data from the long-term study of a discrete natural population of the Seychelles warbler (Acrocephalus sechellensis) on Cousin Island. To our knowledge, this is the first time that GM differences associated with survival have been fully characterised for a natural vertebrate species, across multiple age groups and breeding seasons.Results: We identified substantial variation in GM community structure among sampled individuals, which was partially explained by breeding season (5% of the variance), and host age class (up to 1% of the variance). We also identified significant differences in GM community membership between adult birds that survived, versus those that had died by the following breeding season. Individuals that died carried increased abundances of taxa that are known to be opportunistic pathogens, including several ASVs in the genusMycobacterium. However, there was no association between GM alpha diversity (the diversity of bacterial taxa within a sample) and survival to the next breeding season, or with individual body condition. Additionally, we found no association between GM community membership and individual body condition.Conclusions: These results demonstrate that components of the vertebrate GM can be associated with host fitness in the wild. However, further research is needed to establish whether changes in bacterial abundance contribute to, or are only correlated with, differential survival; this will add to our understanding of the importance of the GM in the evolution of host species living in natural populations.
16 June 2021 in Frontiers in Molecular Biosciences
Streptomyces species are saprophytic soil bacteria that produce a diverse array of specialized metabolites, including half of all known antibiotics. They are also rhizobacteria and plant endophytes that can promote plant growth and protect against disease. Several studies have shown that streptomycetes are enriched in the rhizosphere and endosphere of the model plant Arabidopsis thaliana. Here, we set out to test the hypothesis that they are attracted to plant roots by root exudates, and specifically by the plant phytohormone salicylate, which they might use as a nutrient source. We confirmed a previously published report that salicylate over-producing cpr5 plants are colonized more readily by streptomycetes but found that salicylate-deficient sid2-2 and pad4 plants had the same levels of root colonization by Streptomyces bacteria as the wild-type plants. We then tested eight genome sequenced Streptomyces endophyte strains in vitro and found that none were attracted to or could grow on salicylate as a sole carbon source. We next used 13CO2 DNA stable isotope probing to test whether Streptomyces species can feed off a wider range of plant metabolites but found that Streptomyces bacteria were outcompeted by faster growing proteobacteria and did not incorporate photosynthetically fixed carbon into their DNA. We conclude that, given their saprotrophic nature and under conditions of high competition, streptomycetes most likely feed on more complex organic material shed by growing plant roots. Understanding the factors that impact the competitiveness of strains in the plant root microbiome could have consequences for the effective application of biocontrol strains.
Host‐associated microbiomes are thought to play a key role in host physiology and fitness, but this conclusion mainly derives from systems biased towards animal models and humans. While many studies on non‐model and wild animals have characterised the taxonomic diversity of their microbiomes, few have investigated the functional potential of these microbial communities. Functional ‘omics’ approaches, such as metagenomics, metatranscriptomics and metabolomics, represent promising techniques to probe the significance of host‐associated microbiomes in the wild. In this review, we propose to (1) briefly define the main available functional omics tools along with their strengths and limitations, (2) summarise the key advances enabled by omics tools to understand microbiome function in human and animal models, (3) showcase examples of how these methods have already brought invaluable insights into wild host microbiomes and (4) provide guidelines on how to implement these tools to address outstanding questions in the field of wild animal microbiomes. To conclude, we suggest that, building on knowledge derived from cheaper, more traditional approaches (e.g. 16S metabarcoding and qPCR), functional omics tools represent a promising approach to test hypotheses regarding the ecological and evolutionary significance of the resident microbiota in wild animals. Read the free Plain Language Summary for this article on the Journal blog.
In humans, gut microbiome (GM) differences are often correlated with, and sometimes causally implicated in, ageing. However, it is unclear how these findings translate in wild animal populations. Studies that investigate how GM dynamics change within individuals, and with declines in physiological condition, are needed to fully understand links between chronological age, senescence and the GM, but have rarely been done. Here, we use longitudinal data collected from a closed population of Seychelles warblers (Acrocephalus sechellensis) to investigate how bacterial GM alpha diversity, composition and stability are associated with host senescence. We hypothesised that GM diversity and composition will differ, and become more variable, in older adults, particularly in the terminal year prior to death, as the GM becomes increasingly dysregulated due to senescence. However, GM alpha diversity and composition remained largely invariable with respect to adult age and did not differ in an individual's terminal year. Furthermore, there was no evidence that the GM became more heterogenous in senescent age groups (individuals older than 6 years), or in the terminal year. Instead, environmental variables such as season, territory quality and time of day, were the strongest predictors of GM variation in adult Seychelles warblers. These results contrast with studies on humans, captive animal populations and some (but not all) studies on non‐human primates, suggesting that GM deterioration may not be a universal hallmark of senescence in wild animal species. Further work is needed to disentangle the factors driving variation in GM‐senescence relationships across different host taxa.