Unique and shared responses of the gut microbiota to prolonged fasting: a comparative study across five classes of vertebrate hosts

Abstract

Many animals face unpredictable food sources and periods of prolonged fasting, which likely present significant challenges to gut microorganisms. While several studies have demonstrated that fasting impacts the gut microbiota, experiments have not been carried out in a comparative context. We used 16S rRNA gene sequencing to document changes in colonic and cecal microbiomes of animals representing five classes of vertebrates at four time points through prolonged fasting: tilapia, toads, geckos, quail, and mice. We found differences in the starvation-induced changes in the microbiome across host species and across gut regions. Microbial phylogenetic diversity increased as a result of fasting in the colons of fish, toads, and mice, while quail exhibited a decrease in diversity; geckos exhibited no change. Microbial diversity in the cecum decreased in fish and exhibited no change in mice. Alterations in relative abundances of microbial taxa varied across hosts. Fish exhibited the most significant changes due to fasting, while geckos maintained a stable community over 28 days of fasting. We uncovered several shared responses of the microbiota across hosts. For example, all tetrapods exhibited decreases in the abundances of Coprobacillus and Ruminococcus in response to fasting. We also discuss host-mediated physiological mechanisms that may underlie these community changes.

Integrative Physiology of Fasting

“…Investigatordriven factors can also contribute, including choice of gut segment and microbial community for sampling. At least some of these probably contributed to findings of both unique and common effects of fasting on the diversity and composition of hindgut microbiota of animals from five classes of vertebrates (tilapia, toads, geckos, quail, and mice) (308).…”

The speed and metabolic cost of digesting a blood meal depends on temperature in a major disease vector

“…Although we had not expected to see a change of this magnitude, reductions in SMR of a similar size have been reported in arthropods (Young and Block, 1980; but see Sinclair et al, 2011) and ectothermic vertebrates (Foster and Moon, 1991;Christian et al, 1996;Fuery et al, 1998;McCue, 2007) during prolonged fasting. There are several possible physiological mechanisms to adaptively reduce SMR (reviewed in Storey and Storey, 1990;Hand and Hardewig, 1996) and starvation-induced reductions in the microbial symbionts (sensu Carrero-Colon et al, 2006;Arrese and Soulages, 2010;Kohl et al, 2014) could also underlie changes in metabolic rates. Further research will be needed to determine which of these responses may be occurring in these flies.…”

A place for host–microbe symbiosis in the comparative physiologist's toolbox

“…Some of these 'dedicated' mucindegraders have intimate relationships with host cells and promote processes associated with host health, such as the maintenance of gut barrier function (Reunanen et al, 2015). Retention of beneficial microbes that can degrade host-derived nutrients also promotes ecological stability within the gut community during nutritional deprivation, such as acute or predictable fasts, when metabolic activity of some bacteria is compromised because of an inadequate supply of diet-derived nutrients (Costello et al, 2010;DillMcFarland et al, 2014;Kohl et al, 2015). Species that can degrade host-derived nutrients release intermediate metabolic substrates that other members of the community can use as energy, nitrogen and carbon source -so-called 'cross-feeding' (Seth and Taga, 2014).…”