Ecological rules for the assembly of microbiome communities

Abstract

Humans and many other hosts establish a diverse community of beneficial microbes anew each generation. The order and identity of incoming symbionts is critical for health, but what determines the success of the assembly process remains poorly understood. Here we develop ecological theory to identify factors important for microbial community assembly. Our method maps out all feasible pathways for the assembly of a given microbiome—with analogies to the mutational maps underlying fitness landscapes in evolutionary biology. Building these “assembly maps” reveals a tradeoff at the heart of the assembly process. Ecological dependencies between members of the microbiota make assembly predictable—and can provide metabolic benefits to the host—but these dependencies may also create barriers to assembly. This effect occurs because interdependent species can fail to establish when each relies on the other to colonize first. We support our predictions with published data from the assembly of the preterm infant microbiota, where we find that ecological dependence is associated with a predictable order of arrival. Our models also suggest that hosts can overcome barriers to assembly via mechanisms that either promote the uptake of multiple symbiont species in one step or feed early colonizers. This predicted importance of host feeding is supported by published data on the impacts of breast milk in the assembly of the human microbiome. We conclude that both microbe–microbe and host–microbe interactions are important for the trajectory of microbiome assembly.

Artificial Selection on Microbiomes To Breed Microbiomes That Confer Salt Tolerance to Plants

“…1 ). Based on previous theories ( 5 , 6 , 20 ), such host-mediated indirect selection on microbiomes can be easier than direct selection on microbiomes, particularly with host species that exert strong host control over assembly and stability of their microbiomes ( 6 , 13 , 14 , 21 ).…”

“…Indirect selection is an established breeding technique that can be used when the target trait is difficult or costly to measure ( 11 ), as is the case for microbiome traits compared to the ease of measuring a host phenotype that is dependent on microbiome properties. The efficacy of indirect selection depends on strong correlations between microbiome and host traits; therefore, indirect microbiome selection should be more efficient if such correlations can be maximized experimentally, for example, by controlling ecological priority effects during initial microbiome assembly ( 12 – 15 ) or by increasing host control over microbiome assembly and persistence ( 14 , 16 ). Second, because a typical host likely experienced a long history of evolution to monitor and manipulate its microbiomes (a process called host control) ( 16 – 19 ), indirect microbiome selection uses the host as a kind of thermostat to help gauge and adjust the temperature of its microbiomes, and then propagate desired microbiomes between hosts ( Fig.…”

The role of competition versus cooperation in microbial community coalescence

“…These communities are very complex, typically harboring hundreds of species [5], making them hard to characterize. Over the last decade, the advent of cost-effective high-throughput DNA sequencing techniques has allowed high-resolution mapping of these communities, opening a niche for theoreticians and experimentalists to collaboratively decipher their complexity and assembly [6][7][8][9][10][11][12].…”

The role of competition versus cooperation in microbial community coalescence

“…These communities are very complex, typically harbouring hundreds of species [5], making them hard to characterize. Recently, DNA sequencing has allowed high-resolution mapping of these communities, opening a niche for theoreticians and experimentalists to collaboratively decipher their complexity and assembly [6][7][8][9][10][11]13].…”

“…These communities are very complex, often harbouring hundreds of species [5], making them hard to characterize. Recently, DNA sequencing has allowed a high-resolution mapping of these consortia, opening a niche for theoreticians and experimentalists to collaboratively decipher the complexity of these systems [6][7][8][9][10][11][12][13][14]. Despite thorough explorations, the mechanisms responsible for the assembly of microbial communities have only begun to be revealed.…”