The gastro-intestinal microbiome of organisms is multi-faceted, and consists of a plethora of bacteria, viruses, fungi and archaea that co-evolved with their host. For years, human bacterial gut community have dominated research focus, but recently bacteriophages (viruses infecting bacteria) have been shown to play a vital role in whole community interaction and control. We currently have scant knowledge of the composition or life histories of this portion of the microbiota, especially in non-human organisms. Despite the high ecological and socio-economic value of fish, their gastro-intestinal microbiota, vital to the healthy function of the organism, has received relatively little research interest. Bettarel et al. (2018) aimed to change this, and set out to examine the ecological features of viruses present in the gut microbiome of an extreme euryhaline Tilapia: Sarotherodon melanotheron.
Adult Tilapia were sampled from sites with a range of pollutant concentrations in Senegal, and gut contents were collected. Epifluorescence microscopy was used to quantify bacteria and viruses present; this was compared to numbers in the environment. Viral morphotypes were observed using transmission electron microscopy. The proportion of lysogenic bacteria was also evaluated using a method that manually initiates prophage induction and thus the bacterial lytic cycle, though addition of Mitomycin C (Jiang and Paul, 1996).
This study was the first to report viral abundances in the fish gut, and indeed the community was diverse, abundant (0.2–10.7 x 109 viruses ml-1), and comparable to the human gut. The positive correlation between bacterial and viral abundance suggests viral community was dominated by phages, with an association with the dominant bacterial groups present: Firmicutes, Proteobacteria, and Bacteriodetes. These major members are similar to the human gut microbiome, supporting the paradigm that a core community is needed to ensure efficiency of primary gut function. The rest of the microbiome may be more species-specific to cope with variable diet.
A large proportion (8.1%-33%) of the gut samples consisted of lysogenised bacterial cells (bacterial cells with an integrated viral prophage in the genome), significantly higher than the environmental counterparts. Lysogeny, the non-destructive method of viral reproduction, is usually considered a refuge strategy for viruses in suboptimal environments; for example, when bacterial abundance is low or has compromised metabolism. However, the environment here had a relatively low bacteria : virus ratio due to quickly proliferating bacterial cells, suggesting that a new model, “piggybacking-the-winner”, may be more apt. In this, lysogeny is an advantageous strategy: it can provide immunity against viral sub-infections and improve acquisition of optimal survival genes. Bacterial homeostasis in the gut community is likely to be maintained by having a temperate phageome.
Pollutant concentrations were correlated with the fraction of lysogenised cells, showing that pollutants may be significant in governing the internal microbe-microbe interactions, and so the health of the organism. The physiological stress of their presence could have triggered lysogenic pathways, affecting the balance of temperate and virulent viruses in the gut microbiome, compromising the carefully balanced equilibrium.
This study not only sheds light on a little known portion of an important microbial system, but also provides further stock to the “piggybacking-the-winner” strategy. The notion that processes can have multiple uses within different ecological contexts is an important one, and one which incurs curiosity in every instance: more research into this will undoubtedly lead to exciting discoveries!
Reviewed paper:
Bettarel, Y., Combe, M., Adingra, A., Ndiaye, A., Bouvier, T., Panfili, J., & Durand, J. D. (2018). Hordes of Phages in the Gut of the Tilapia Sarotherodon melanotheron. Scientific reports, 8.
Jiang, S. C., & Paul, J. H. (1996). Occurrence of lysogenic bacteria in marine microbial communities as determined by prophage induction. Marine Ecology Progress Series, 142, 27-38.
This is really useful for the growing industry of Talapia in acquaponics. So, the theories that we thought were previously true about lysogenic/lytic interactions are far more complex than we thought! Also, I didn't realise that human and fish gut biota were so similar!
ReplyDeleteIt would be really interesting to see how (if at all) the gut microbiome of the Tilapia influences the growth/efficiency of the nitrifying bacteria and plants in this system! I guess that there is a reasonable proportion of the gut viral community that is transient, or at least renewed on occasion, so I suppose some of it would reach the bacteria/plants in the rest of the system. Perhaps this interaction would even further complicate the lysogenic/lytic cycle and affect the rest of the assemblage? Ecology is a complicated one...
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