Knowing your friends: invertebrate innate immunity fosters beneficial bacterial symbioses

Abstract

The innate immune system is present in all animals and is a crucial first line of defence against pathogens. However, animals also harbour large numbers of beneficial microorganisms that can be housed in the digestive tract, in specialized organs or on tissue surfaces. Although invertebrates lack conventional antibody-based immunity, they are capable of eliminating pathogens and, perhaps more importantly, discriminating them from other microorganisms. This Review examines the interactions between the innate immune systems of several model invertebrates and the symbionts of these organisms, and addresses the central question of how these long-lived and specific associations are established and maintained.

Ontogenetic Changes in the Bacterial Symbiont Community of the Tropical Demosponge Amphimedon queenslandica: Metamorphosis Is a New Beginning

“…Innate immune genes are of interest because of their hypothesized roles in invertebrates in establishing and maintaining bacterial symbiont communities (Nyholm and Graf, 2012). As discussed above, both our histological data and that of other studies report that phagocytosis of symbionts can occur at least during the larval stage in some sponge species (Ereskovsky and Tokina, 2004;de Caralt et al, 2007).…”

Hemolymph Melanization in the Silkmoth Bombyx mori Involves Formation of a High Molecular Mass Complex That Metabolizes Tyrosine

“…Another possibility is that damaged cuticle could also release factors that activate the PO cascade, given that 1) the first PAP identified from B. mori was purified from cuticle rather than hemolymph, and 2) studies from other invertebrates have identified molecules from damaged ectoderm that trigger immune defenses (17,51,52). In contrast, if microbes on the surface of B. mori larvae or signals released from damaged cuticle activate the rapid melanization of B. mori plasma, it remains unclear why plasma from species like M. sexta or T. molitor does not behave similarly because intuitively we would expect commensal microbes to reside on the surface of all arthropods.…”

Friend, foe or food? Recognition and the role of antimicrobial peptides in gut immunity and Drosophila –microbe interactions

“…Comparisons between flies grown in the absence of gut microbiota (axenic) and conventionally reared flies have shown multiple contributions of bacteria to adult physiology, including lipid storage and glucose levels [58,70,71], gut stem cell activity [42,63], mating preference [72] and disease susceptibility [61,73]. Moreover, as discussed in greater detail below, as in other animals [1,2,7], the microbiota of D. melanogaster is also important for maturation of host immune and stress responses [3,13,14,21], and the gut epithelial immune response is considered an important regulator of microbiota composition and density [35,42,63,74].…”

“…Alterations in the microbiome (i.e. composition, density or function) are linked to a number of diseases and the innate immune system has a central role in regulating these associations [1,2,7,8]. The recognition of microbeassociated molecular patterns (MAMPs) by pattern recognition receptors (PRRs) and subsequent production of antimicrobial peptides (AMPs) are evolutionarily conserved and a major component of the host epithelial response to both beneficial and pathogenic microorganisms [9].…”

“…While this also makes the gut an important entry point for pathogens, the animal gut is most typically in constant association with a microbiota and these interactions have important roles in animal biology [1,2]. Comparisons between germ-free and conventional-reared animals have demonstrated that gut microbiota have significant impacts on diverse host functions, including: development, the establishment and function of the mucosal immune system, epithelial morphogenesis, as well as systemic impacts on host metabolism and endocrine pathways through the gut -brain axis [3][4][5][6].…”