Not all animals need a microbiome

Abstract

It is often taken for granted that all animals host and depend upon a microbiome, yet this has only been shown for a small proportion of species. We propose that animals span a continuum of reliance on microbial symbionts. At one end are the famously symbiont-dependent species such as aphids, humans, corals and cows, in which microbes are abundant and important to host fitness. In the middle are species that may tolerate some microbial colonization but are only minimally or facultatively dependent. At the other end are species that lack beneficial symbionts altogether. While their existence may seem improbable, animals are capable of limiting microbial growth in and on their bodies, and a microbially independent lifestyle may be favored by selection under some circumstances. There is already evidence for several ‘microbiome-free’ lineages that represent distantly related branches in the animal phylogeny. We discuss why these animals have received such little attention, highlighting the potential for contaminants, transients, and parasites to masquerade as beneficial symbionts. We also suggest ways to explore microbiomes that address the limitations of DNA sequencing. We call for further research on microbiome-free taxa to provide a more complete understanding of the ecology and evolution of macrobe-microbe interactions.

Bacterial communities of herbivores and pollinators that have co-evolved Cucurbita spp

“…The high number of rare, low abundance OTUs in Acalymma herbivores is consistent with accumulating evidence that the local environment – ie , the variable and diverse microbial communities that colonize plants or the surrounding soil – are the most significant source of microbial exposure for most non-social and non-sap feeding insects (Moran 2003, Kwong and Moran 2016, Hammer et al 2017, McFrederick et al 2017, Hammer et al 2019, Hannula et al 2019). The lower average number of OTUs per insect in bees compared to beetles may reflect that bees exclusively feed on Cucurbita floral resources, while Acalymma beetles are often found feeding on other introduced cucurbit crop plants (most notably muskmelon and cucumbers, both Cucumis spp.…”

“…The large geographic area from which beetles were sampled may also contribute to the high number of rare OTUs. Overall, the composition and diversity patterns reflect that Acalymma beetles are transiently exposed to diverse bacteria that do not persistently colonize them as hosts (Hammer et al 2017, Hammer et al 2019).…”

“…Herbivorous insects that consume leaf, floral, stem or root tissues are exposed to diverse communities of microbes associated with plants and/or soil. Many microbes ingested by insects likely pass transiently through the digestive tract and may not confer any impact on the host insect (Oliver et al 2008, Hammer et al 2017, Hammer et al 2019). However, some microbes are able to colonize insects as hosts, and can have diverse and consequential – yet often cryptic – roles in mediating ecological interactions between plants, other insects and other microbes (Shapiro et al 2012, Chung et al 2013, Shapiro et al 2013, Wang et al 2016, Mason et al2018).…”

The microbiome of theMelitaea cinxiabutterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant

“…Endosymbionts can also protect their hosts against abiotic stressors and pathogens (Montllor et al, 2002;Dunbar et al, 2007;King et al, 2016). The literature may, however, be biased towards mutualistic and parasitic/pathogenic interactions, as commensal or neutral interactions may be understudied or underreported (reviewed by Hammer et al, 2019). In general, the microbiota is a multilayer system in which prevalent members compose the core microbiota and a more flexible pool of microbial members compose the non-core community (Shapira, 2016).…”

Contrasting Strategies: Human Eukaryotic Versus Bacterial Microbiome Research

“…A few interesting exceptions include David et al (2014), who detected many foodborne bacteria and fungi (some of which expressed genes), and Minot et al (2011), who took transience into account for viruses in the gut. It is now better recognized that numerous insects do not have resident bacterial microbiota, and that this has important implications for bacterial community stability, host fitness and mutualism (Hammer et al 2017(Hammer et al , 2019Ross et al 2018). Recognizing this issue earlier in the development of eukaryotic microbiome research may allow more fine-grained ecological and evolutionary insight into microbiota dynamics.…”