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ABSTRACT Reef-building corals depend on symbiosis with photosynthetic algae that reside within their cells. As important as this relationship is for maintaining healthy reefs, it is strikingly delicate. When ocean temperatures briefly exceed the average summer maximum, corals can bleach, losing their endosymbionts. Although the mechanisms governing bleaching are unknown, studies implicate uncoupling of coral and algal cell divisions at high temperatures. Still, little is known regarding the coordination of host and algal cell divisions. Control of nutrient exchange is one likely mechanism. Both nitrogen and phosphate are necessary for dividing cells, and although nitrogen enrichment is known to increase symbiont density in the host, the consequences of phosphate enrichment are poorly understood. Here, we examined the effects of phosphate depletion on symbiont growth in culture and compared the physiology of phosphate-starved symbionts in culture to symbionts that were freshly isolated from a host. We found that available phosphate is as low in freshly isolated symbionts as it is in phosphate-starved cultures. Furthermore, RNAseq revealed that phosphate-limited and freshly isolated symbionts have similar patterns of gene expression for phosphate-dependent genes, most notably upregulation of phosphatases, which is consistent with phosphate recycling. Similarly, lipid profiling revealed a substantial decrease in phospholipid abundance in both phosphate-starved cultures and freshly isolated symbionts. These findings are important because they suggest that limited access to phosphate controls algal cell divisions within a host. IMPORTANCEThe corals responsible for building tropical reefs are disappearing at an alarming rate as elevated sea temperatures cause them to bleach and lose the algal symbionts they rely on. Without these symbionts, corals are unable to harvest energy from sunlight and, therefore, struggle to thrive or even survive in the nutrient-poor waters of the tropics. To devise solutions to address the threat to coral reefs, it is necessary to understand the cellular events underpinning the bleaching process. One model for bleaching proposes that heat stress impairs algal photosynthesis and transfer of sugar to the host. Consequently, the host’s demands for nitrogen decrease, increasing nitrogen availability to the symbionts, which leads to an increase in algal proliferation that overwhelms the host. Our work suggests that phosphate may play a similar role to nitrogen in this feedback loop. 

ABSTRACT Herbivores must overcome a variety of plant defenses, including coping with plant secondary compounds (PSCs). To help detoxify these defensive chemicals, several insect herbivores are known to harbor gut microbiota with the metabolic capacity to degrade PSCs. Leaf-cutter ants are generalist herbivores, obtaining sustenance from specialized fungus gardens that act as external digestive systems and which degrade the diverse collection of plants foraged by the ants. There is in vitro evidence that certain PSCs harm Leucoagaricus gongylophorus , the fungal cultivar of leaf-cutter ants, suggesting a role for the Proteobacteria -dominant bacterial community present within fungus gardens. In this study, we investigated the ability of symbiotic bacteria present within fungus gardens of leaf-cutter ants to degrade PSCs. We cultured fungus garden bacteria, sequenced the genomes of 42 isolates, and identified genes involved in PSC degradation, including genes encoding cytochrome P450 enzymes and genes in geraniol, cumate, cinnamate, and α-pinene/limonene degradation pathways. Using metatranscriptomic analysis, we showed that some of these degradation genes are expressed in situ . Most of the bacterial isolates grew unhindered in the presence of PSCs and, using gas chromatography-mass spectrometry (GC-MS), we determined that isolates from the genera Bacillus , Burkholderia , Enterobacter , Klebsiella , and Pseudomonas degrade α-pinene, β-caryophyllene, or linalool. Using a headspace sampler, we show that subcolonies of fungus gardens reduced α-pinene and linalool over a 36-h period, while L. gongylophorus strains alone reduced only linalool. Overall, our results reveal that the bacterial communities in fungus gardens play a pivotal role in alleviating the effect of PSCs on the leaf-cutter ant system. IMPORTANCE Leaf-cutter ants are dominant neotropical herbivores capable of deriving energy from a wide range of plant substrates. The success of leaf-cutter ants is largely due to their external gut, composed of key microbial symbionts, specifically, the fungal mutualist L. gongylophorus and a consistent bacterial community. Both symbionts are known to have critical roles in extracting energy from plant material, yet comparatively little is known about their roles in the detoxification of plant secondary compounds. In this study, we assessed if the bacterial communities associated with leaf-cutter ant fungus gardens can degrade harmful plant chemicals. We identify plant secondary compound detoxification in leaf-cutter ant gardens as a process that depends on the degradative potential of both the bacterial community and L. gongylophorus . Our findings suggest that the fungus garden and its associated microbial community influence the generalist foraging abilities of the ants, underscoring the importance of microbial symbionts in plant substrate suitability for herbivores. 

ABSTRACT Commensal microbial communities have immense effects on their vertebrate hosts, contributing to a number of physiological functions, as well as host fitness. In particular, host immunity is strongly linked to microbiota composition through poorly understood bi-directional links. Gene expression may be a potential mediator of these links between microbial communities and host function. However, few studies have investigated connections between microbiota composition and expression of host immune genes in complex systems. Here, we leverage a large study of laboratory-raised fish from the species Gasterosteus aculeatus (three-spined stickleback) to document correlations between gene expression and microbiome composition. First, we examined correlations between microbiome alpha diversity and gene expression. Our results demonstrate robust positive associations between microbial alpha diversity and expression of host immune genes. Next, we examined correlations between host gene expression and abundance of microbial taxa. We identified 15 microbial families that were highly correlated with host gene expression. These families were all tightly correlated with host expression of immune genes and processes, falling into one of three categories—those positively correlated, negatively correlated, and neutrally related to immune processes. Furthermore, we highlight several important immune processes that are commonly associated with the abundance of these taxa, including both macrophage and B cell functions. Further functional characterization of microbial taxa will help disentangle the mechanisms of the correlations described here. In sum, our study supports prevailing hypotheses of intimate links between host immunity and gut microbiome composition. IMPORTANCE Here, we document associations between host gene expression and gut microbiome composition in a nonmammalian vertebrate species. We highlight associations between expression of immune genes and both microbiome diversity and abundance of specific microbial taxa. These findings support other findings from model systems which have suggested that gut microbiome composition and host immunity are intimately linked. Furthermore, we demonstrate that these correlations are truly systemic; the gene expression detailed here was collected from an important fish immune organ (the head kidney) that is anatomically distant from the gut. This emphasizes the systemic impact of connections between gut microbiota and host immune function. Our work is a significant advancement in the understanding of immune-microbiome links in nonmodel, natural systems.