Missing symbionts: do some animals lack resident gut microbiomes?

It seems like the field of “gut microbiomics” is having major breakthroughs almost every month these days. It’s very exciting to follow what is being discovered and gut microbes have now been linked with an array of important host traits, such as health, disease resistance, digestion, behavior, and longevity. The more one reads about gut bacteria and other microbes, the more convinced one gets of their importance for animals as hosts.
However, evidence are starting to emerge as to question whether all animals truly harbor gut microbiomes. Tobin Hammer and colleagues recently published a paper in PNAS where they laid out the case for the missing gut microbiomes of caterpillars. Hammer et al. (2017) sequenced guts and feces from 124 leaf-eating caterpillar species of 15 families and found unusually low densities of bacteria and fungal microbes present in their guts. Most bacteria present were highly similar to the ones present on their food (plant leaves), and therefore only transient and not residing in the caterpillar gut.

Figure 1 from Hammer et al. Comparisons of bacterial density, relative abundance of plant DNA, and intraspecific variability between caterpillars and other animals expected to host functional microbiomes. Please see the paper for detailed description. 

Of course, absence of evidence is not evidence of absence, as the authors are well aware of. They therefore included comparisons in their study to a range of other vertebrates and invertebrates. In addition, they carried out antibiotic treatments of Manduca sexta caterpillars to evaluate if wiping out their present low-level plant-associated bacteria would affect their development. That experiment showed no differences in e.g. pupal weight, development time, and survival between the antibiotic treatments and controls, a result further strengthening their hypothesis of no or extremely few resident microbes within the guts of caterpillars.
This study, together with others that report the apparent absence of microbes in caterpillar guts, naturally raises the question if other animals lack gut microbiomes as well? Even though they often are more simple compared to those of vertebrates, we know that insects such as honey bees and mosquitoes harbor gut microbiomes. Ants too, though some seem to harbor very few, only marginally above detection limits (Sanders et al. 2017). My guess is that we in the near future will see more evidence of missing microbes in animals, and I look forward to future studies investigating just why some hosts seem to do just fine without gut symbionts.
Tobin J. Hammer, Daniel H. Janzen, Winnie Hallwachs, Samuel P. Jaffe, and Noah Fierer. Caterpillars lack a resident gut microbiome. PNAS, 2017; published ahead of print. August 22, 2017, doi:10.1073/pnas.1707186114
Jon G. Sanders, Piotr Łukasik, Megan E. Frederickson, Jacob A. Russell, Ryuichi Koga, Rob Knight, Naomi E. Pierce. Dramatic Differences in Gut Bacterial Densities Correlate with Diet and Habitat in Rainforest Ants. Integrative and Comparative Biology, 2017. https://doi.org/10.1093/icb/icx088

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