Building the microbiome in health and disease: niche construction and social conflict in bacteria

Abstract

Microbes collectively shape their environment in remarkable ways via the products of their metabolism. The diverse environmental impacts of macro-organisms have been collated and reviewed under the banner of 'niche construction'. Here, we identify and review a series of broad and overlapping classes of bacterial niche construction, ranging from biofilm production to detoxification or release of toxins, enzymes, metabolites and viruses, and review their role in shaping microbiome composition, human health and disease. Some bacterial niche-constructing traits can be seen as extended phenotypes, where individuals actively tailor their environment to their benefit (and potentially to the benefit of others, generating social dilemmas). Other modifications can be viewed as non-adaptive by-products from a producer perspective, yet they may lead to remarkable within-host environmental changes. We illustrate how social evolution and niche construction perspectives offer complementary insights into the dynamics and consequences of these traits across distinct timescales. This review highlights that by understanding the coupled bacterial and biochemical dynamics in human health and disease we can better manage host health.

Keywords: community ecology; cooperation; microbiota; niche construction; social evolution.

Figure 1.

Social calculus for costly secreted factors is dependent on density and mixing of a population. Focal cell and focal cell niche-constructing behaviours are shown in black, interactants are shown in grey. (a–c) Secreted public good molecule (e.g. iron-scavenging siderophore or extracellular digestive enzyme). (d) Lytically produced anti-competitor toxin (e.g. bacteriocin).

Figure 2.

The niche construction effect of bile acid modification by C. scindens. Dehydroxylation of bile acids by C. scindens at the caecum (upper colon) leads to suppression of C. difficile in the lower colon. Bile acid modification may directly yield energy for C. scindens, but may also suppress the growth of local competitors, which could be an adaptive or incidental function. Finally, the downstream effect of C. scindens on C. difficile may either provide benefits via immune system interaction or may be incidental.