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Bee microbiomes go viral
Friday, 2020/05/29 | 08:27:14

Waldan K. Kwong; PNAS May 26, 2020 117 (21) 11197-11199

Figure: A diverse array of bacterial species and strains (different colors) in the bee gut act as hosts for different bacteriophages. Phages can be specific to multiple bacterial strains, and bacteria can be susceptible to multiple phages.


Perhaps now more than ever (1), it is abundantly clear that viruses can rapidly and dramatically alter host populations, both by direct mortality and by changing the way hosts interact with each other. Like macroscopic organisms, bacteria also contend with their own viruses. Called bacteriophages (or simply, phages), these nanometer-scale parasites are the most numerous, yet least well-characterized, forms of “life” on the planet (23). Because of their inability to directly grow phages (or most of their bacterial hosts), researchers have had only a limited view of the abundance, distribution, and population structure of phage communities. Now, a pair of studies in PNAS, by Bonilla-Rosso et al. (4) and Deboutte et al. (5), have pulled back the curtain on the phages of an emerging model microbiome system: that of the bee gut.


Honey bees (Apis mellifera), like humans, have a uniquely specialized gut microbiome that has developed over millions of years of coevolution (6). A billion cells strong, the bacteria within each bee play significant roles in extracting dietary nutrients and fending off pathogens (711). If what we know from mammalian gut microbiomes holds (12), there also exist as many phages as bacteria in the bee gut. However, to date, there has been no unbiased systematic survey of phages from bees. Both Bonilla-Rosso et al. (4) and Deboutte et al. (5) ambitiously set out to use metagenomic sequencing on viral particles purified from bees, to offer a glimpse into the diversity of phages present as well as the types of genes they carry.


Bonilla-Rosso et al. (4) combined hundreds of bees from Swiss hives into two samples for analysis, whereas Deboutte et al. (5) used two to six bees from multiple hives across Belgium, for a total of 102 samples. After sequencing extremely deeply, at up to several billion DNA bases per sample, both studies come to a similar striking conclusion: that most of the phages [76% (4) and 91% (5)] in bees are unclassifiable. In other words, they represent viruses that have never been seen before. Of the sequences that could be classified, the majority fall into three families of tailed phages, the Myoviridae, Siphoviridae, and Podoviridae. What’s more, when Deboutte et al. (5) plot the number of unique phages discovered as a function of their extensive sampling effort—a species accumulation curve—they find no sign of a plateau, indicating that what these two studies uncovered are but a miniscule portion of a vast pool of phage diversity in bees.


Even the approach of sequencing purified viral particles gives merely a limited impression of the phage community. This is because phages can engage in two different lifestyles: lytic and temperate (lysogenic). Lytic phages, upon infecting bacteria, rapidly undergo reproduction, eventually bursting their host and releasing more phage particles. In contrast, temperate phages integrate their genetic material into the host bacterium’s chromosome and can lie dormant for many host generations. To find the phages lying within bacterial genomes, Bonilla-Rosso et al. (4) analyzed the bacterial metagenomes of 73 individual honey bees from Switzerland and Japan. They discovered that about half of the diversity in the viral particles they sequenced came from temperate phages; however, in terms of sheer abundance, ∼90% of viral particles were suspected to be from lytic phages. Hence, the dynamics of the lytic and temperate portions of the bee phage community could be quite distinct. Bonilla-Rosso et al. (4) noticed that the phages in their bacterial metagenomes (which were dominated by temperate phages) were generally conserved across sampling times and even between bees from Europe and Asia. However, the lytic phages were much more variable (4), and analysis of viral particle samples (which were presumably dominated by lytic phages) by Deboutte et al. (5) finds that phage compositions vary with both geographic location and sampling date. They further determined that the phages present in any given sample were usually found in fewer than 5 other samples, of 102 total samples. Altogether, these data indicate that phage populations—at least in terms of those existing as viral particles—can be highly dynamic between individual bees and across geographic and temporal scales.


The disposition of phages is also inexorably linked to that of their hosts, the resident bacteria of the bee gut. Both studies seek to assign phages to hosts, taking advantage of the fact that many bee gut bacteria have already been cultured and genome sequenced (45). Using genome-encoded prophages, transfer RNAs, and CRISPR spacers as clues, they identified phages targeting all of the major bacterial groups in the bee microbiome, with most of the host-assignable viral particles targeting the genera BifidobacteriumLactobacillus, and Gilliamella. Bonilla-Rosso et al. (4) further isolated eight strains of phages from their collection of viral particles. After testing against a slate of >100 bee gut bacteria cultures, they found that all eight phages infected Bifidobacterium strains; however, there are stark differences in the susceptibility of different bacterial strains to the different viral strains. Even more intriguingly, differences in susceptibility are often most drastic between closely related Bifidobacterium. This insinuates that phages have some sort of mutable specificity for their hosts (Fig. 1) and highlights how little we know about the factors governing phage−bacteria interactions.


Phages are undoubtedly important agents of change in gut microbial communities, but how exactly they affect the microbiome, and, by extension, the animals that house them, largely remains a mystery. Potential mechanisms include direct killing, triggering of immunological responses, and fostering gene transfer between cells (20). Studying such factors in honey bees and other emerging model systems will provide much-needed novel perspectives into these tiniest members of the microbiome. Ultimately, understanding viral dynamics will be key to predicting and improving host outcomes, whether in humans or in bees.


See https://www.pnas.org/content/117/21/11197

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