In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal–bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other’s genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal–bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world
Mammalian hibernators undergo a remarkable phenotypic switch that involves profound changes in physiology, morphology, and behavior in response to periods of unfavorable environmental conditions. The ability to hibernate is found throughout the class Mammalia and appears to involve differential expression of genes common to all mammals, rather than the induction of novel gene products unique to the hibernating state. The hibernation season is characterized by extended bouts of torpor, during which minimal body temperature (Tb) can fall as low as -2.9 degrees C and metabolism can be reduced to 1% of euthermic rates. Many global biochemical and physiological processes exploit low temperatures to lower reaction rates but retain the ability to resume full activity upon rewarming. Other critical functions must continue at physiologically relevant levels during torpor and be precisely regulated even at Tb values near 0 degrees C. Research using new tools of molecular and cellular biology is beginning to reveal how hibernators survive repeated cycles of torpor and arousal during the hibernation season. Comprehensive approaches that exploit advances in genomic and proteomic technologies are needed to further define the differentially expressed genes that distinguish the summer euthermic from winter hibernating states. Detailed understanding of hibernation from the molecular to organismal levels should enable the translation of this information to the development of a variety of hypothermic and hypometabolic strategies to improve outcomes for human and animal health.
Mammalian hibernation consists of torpor phases when metabolism is severely depressed, and T(b) can reach as low as approximately -2°C, interrupted by euthermic arousal phases. Hibernation affects the function of the innate and the adaptive immune systems. Torpor drastically reduces numbers of all types of circulating leukocytes. In addition, other changes have been noted, such as lower complement levels, diminished response to LPS, phagocytotic capacity, cytokine production, lymphocyte proliferation, and antibody production. Hibernation may therefore increase infection risk, as illustrated by the currently emerging WNS in hibernating bats. Unraveling the pathways that result in reduced immune function during hibernation will enhance our understanding of immunologic responses during extreme physiological changes in mammals.
Many hibernating mammals suspend food intake during winter, relying solely on stored lipids to fuel metabolism. Winter fasting in these species eliminates a major source of degradable substrates to support growth of gut microbes, which may affect microbial community structure and host-microbial interactions. We explored the effect of the annual hibernation cycle on gut microbiotas using deep sequencing of 16S rRNA genes from ground squirrel cecal contents. Squirrel microbiotas were dominated by members of the phyla Bacteroidetes, Firmicutes, and Verrucomicrobia. UniFrac analysis showed that microbiotas clustered strongly by season, and maternal influences, diet history, host age, and host body temperature had minimal effects. Phylogenetic diversity and numbers of operational taxonomic units were lowest in late winter and highest in the spring after a 2-wk period of refeeding. Hibernation increased relative abundance of Bacteroidetes and Verrucomicrobia, phyla that contain species capable of surviving on host-derived substrates such as mucins, and reduced relative abundance of Firmicutes, many of which prefer dietary polysaccharides. Hibernation reduced cecal short-chain fatty acid and ammonia concentrations, and increased and decreased concentrations of acetate and butyrate, respectively. These results indicate that the ground squirrel microbiota is restructured each year in a manner that reflects differences in microbial preferences for dietary vs. host-derived substrates, and thus the competitive abilities of different taxa to survive in the altered environment in the hibernator gut.
Dramatic changes in blood flow occur during torpor-arousal cycles in mammalian hibernators that could increase the risk of oxidative stress to sensitive tissues. We used 13-lined ground squirrels (Spermophilus tridecemlineatus) to determine the effect of hibernation on lipid peroxidation and expression of stress-activated signaling pathways in the intestine, a tissue highly susceptible to ischemia-reperfusion injury. Compared with summer-active squirrels, levels of the mitochondrial stress protein GRP75 were consistently higher in intestinal mucosa of hibernators in each of five hibernation states (entrance, short-bout torpid, long-bout torpid, arousal and interbout euthermia). The redox-sensitive transcription factor, nuclear factor-kappaB (NF-kappaB), was strongly activated in each hibernation state compared with summer squirrels except for squirrels during an arousal from torpor. In contrast, NF-kappaB activation in brown adipose tissue (BAT) was low in active and hibernating squirrels regardless of season. Levels of conjugated dienes (products of lipid peroxidation) were higher in intestine of hibernators entering torpor and early in a torpor bout compared with summer squirrels. Conjugated diene levels were also higher in short-bout torpid vs arousing squirrels. The results suggest that the intestinal mucosa is vulnerable to oxidative stress during the hibernation season and in response may activate cellular defense pathways that help minimize severe oxidative damage induced by torpor-arousal cycles.
Extended bouts of fasting are ingrained in the ecology of many organisms, characterizing aspects of reproduction, development, hibernation, estivation, migration, and infrequent feeding habits. The challenge of long fasting episodes is the need to maintain physiological homeostasis while relying solely on endogenous resources. To meet that challenge, animals utilize an integrated repertoire of behavioral, physiological, and biochemical responses that reduce metabolic rates, maintain tissue structure and function, and thus enhance survival. We have synthesized in this review the integrative physiological, morphological, and biochemical responses, and their stages, that characterize natural fasting bouts. Underlying the capacity to survive extended fasts are behaviors and mechanisms that reduce metabolic expenditure and shift the dependency to lipid utilization. Hormonal regulation and immune capacity are altered by fasting; hormones that trigger digestion, elevate metabolism, and support immune performance become depressed, whereas hormones that enhance the utilization of endogenous substrates are elevated. The negative energy budget that accompanies fasting leads to the loss of body mass as fat stores are depleted and tissues undergo atrophy (i.e., loss of mass). Absolute rates of body mass loss scale allometrically among vertebrates. Tissues and organs vary in the degree of atrophy and downregulation of function, depending on the degree to which they are used during the fast. Fasting affects the population dynamics and activities of the gut microbiota, an interplay that impacts the host's fasting biology. Fasting-induced gene expression programs underlie the broad spectrum of integrated physiological mechanisms responsible for an animal's ability to survive long episodes of natural fasting.
lined ground squirrels and other circannual hibernators undergo profound physiological changes on an annual basis, transitioning from summer homeothermy [body temperature (Tb) ϳ37°C] to winter heterothermy (Tb cycling between 0°C and 37°C). We hypothesize that these physiological changes are reflected in biochemical changes that provide mechanistic insights into, and biomarkers for, hibernation states. Here we report the results of an NMR-based metabolomics analysis of liver extracts from ground squirrels in three distinct physiological states of circannual hibernation: summer active (SA), late torpor (LT), and reentering torpor (Ent) after one of the euthermic arousals. Of the 43 identified and quantified metabolites, 36 differed among these three states and fell into two patterns of variation: 1) SA differed from both of the two winter states; or 2) the two winter states differed from each other, but one of the two was not different from SA. Concentrations of hepatic glucose, lactate, alanine, succinate, -hydroxybutyrate, glutamine, and betaine were identified as robust hepatic biomarkers that together distinguish among animals in these three states of the circannual hibernation rhythm. These data are consistent with a proposed two-switch model of hibernation, in which setting the summer-winter switch to winter enables expression of a distinct torpor-arousal switch. The summer-winter switch is characterized by the metabolites associated with the well-known switch from carbohydrate to lipid fuel utilization during hibernation. The torpor-arousal switch is characterized by the accumulation of metabolites of nitrogen (glutamine) and phospholipid (betaine) catabolism in LT with the capacity to act as protective osmolytes. metabolomics; nitrogen metabolism; osmolytes; Spermophilus tridecemlineatus; torpor MAMMALIAN HIBERNATORS are uniquely able to orchestrate and survive extended periods of extremely low body temperature (T b ) and metabolic, respiratory, and heart rates in a state called torpor. The deep, multiday periods of torpor that characterize hibernation alternate with periodic short arousals that reverse the dramatic physiological depressions associated with the torpid state (reviewed in Ref. 5). Thus hibernators, including 13-lined ground squirrels (Spermophilus tridecemlineatus), are homeothermic like most mammals in summer but switch to heterothermy in winter (Fig. 1). The biochemical consequences of periodic arousals from torpor are complex and come with tremendous costs. Although hibernation is a strategy that saves large amounts of energy over the winter compared with remaining euthermic (ϳ90%), most of the energy used in winter (Ͼ70%) is used to fuel these interbout arousals (Ref. 22 and references therein). Hence the arousals are an enigma-Why arouse when remaining torpid would save so much more energy? It has been suggested that hibernators must rewarm to restore or remove a metabolic imbalance (Ref. 27, chapter 6).Metabolomics seeks to identify and quantify the low-molecular-weight endogenous co...
Fasting or malnutrition (FM) has dramatic effects on small intestinal mucosal structure and transport function. Intestinal secretion of ions and fluid is increased by FM both under basal conditions and in response to secretory agonists. Intestinal permeability to ions and macromolecules may also be elevated by FM, which increases the potential for fluid and electrolyte losses and for anaphylactic responses to luminal antigens. Mucosal atrophy induced by FM reduces total intestinal absorption of nutrients, but nutrient absorption normalized to mucosal mass may actually be enhanced by a variety of mechanisms, including increased transporter gene expression, electrochemical gradients, and ratio of mature to immature cells. These observations underscore the value of enteral feeding during health and disease.
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.
hi@scite.ai
334 Leonard St
Brooklyn, NY 11211
Copyright © 2024 scite LLC. All rights reserved.
Made with 💙 for researchers
Part of the Research Solutions Family.