A new lexicon in the age of microbiome research

Abstract

At a rapid pace, biologists are learning the many ways in which resident microbes influence, and sometimes even control, their hosts to shape both health and disease. Understanding the biochemistry behind these interactions promises to reveal completely novel and targeted ways of counteracting disease processes. However, in our protocols and publications, we continue to describe these new results using a language that originated in a completely different context. This language developed when microbial interactions with hosts were perceived to be primarily pathogenic, as threats that had to be vanquished. Biomedicine had one dominating thought: winning this war against microorganisms. Today, we know that beyond their defensive roles, host tissues, especially epithelia, are vital to ensuring association with the normal microbiota, the communities of microbes that persistently live with the host. Thus, we need to adopt a language that better encompasses the newly appreciated importance of host-microbiota associations. We also need a language that frames the onset and progression of pathogenic conditions within the context of the normal microbiota. Such a reimagined lexicon should make it clear, from the very nature of its words, that microorganisms are primarily vital to our health, and only more rarely the cause of disease. This article is part of the theme issue ‘Sculpting the microbiome: how host factors determine and respond to microbial colonization’.

When the microbiome shapes the host: immune evolution implications for infectious disease

“…In natural settings, opportunistic systemic infections probably occur alongside parasite attack, as many Drosophila parasites pierce the cuticle of fly larvae that are, quite literally, swimming in Acetobacter . The context deciding whether a microbe is a mutualist or pathogen can therefore be defined by the presence of just a single AMP–indeed, the use of such labels is discussed in [ 51 ]. A similarly specific interaction was previously shown for a beetle peptide in control of its coevolving symbiont housed in specialized host tissue [ 52 ].…”

Novel technologies uncover novel ‘anti’-microbial peptides in Hydra shaping the species-specific microbiome

“…For several decades, it has been accepted that AMPs, as ‘killers’ and hence often referred to as host-defence peptides (HDP; [ 70 ]), protect an animal from noxious microorganisms. More recently, as stated above, we start appreciating a broader role of AMPs in shaping the commensal microbiome [ 71 ]. The Hydra host imposes strong selective forces on its microbiome via section of diverse AMPs [ 72 ] and thereby maintains species-specific microbiota communities over extended periods [ 12 , 63 , 73 ].…”

“…As outlined in detail in another paper in this issue [ 98 ], from the beginning of animal (and plant) evolution, AMPs serve a crucial role in regulating the composition of the microbiome [ 1 ]. These findings make it quite clear that AMPs do much more than just kill pathogens.…”

Sculpting the microbiome

“…Reflecting on this, the issue closes with an essay by Bosch et al . [ 17 ] on the language we use to frame studies of host–microbe interactions. Host–microbe interactions have long adopted the language of war, situated in a framework of host–pathogen conflict.…”

“…Bosch et al . [ 17 ] provide a broader scope with which to view host–microbe systems, and propose updates to the lexicon we use that better acknowledge the diverse and content-dependent roles that host genes and microbial factors have in organismal health.…”