Abstract

The study of the forces which govern the geographical distributions of life is known as biogeography, a subject which has fascinated zoologists, botanists and ecologists for centuries. Advances in our understanding of community ecology and biogeography—supported by rapid improvements in next generation sequencing technology—have now made it possible to identify and explain where and why life exists as it does, including within the microbial world. In this review, we highlight how a unified model of microbial biogeography, one which incorporates the classic ecological principles of selection, diversification, dispersion and ecological drift, can be used to explain community dynamics in the settings of both health and disease. These concepts operate on a multiplicity of temporal and spatial scales, and together form a powerful lens through which to study microbial population structures even at the finest anatomical resolutions. When applied specifically to curious strains of conjunctivitis-causing, nonencapsulated Streptococcus pneumoniae, we show how this conceptual framework can be used to explain the possible evolutionary and disease-causing mechanisms which allowed these lineages to colonize and invade a separate biogeography. An intimate knowledge of this radical bifurcation in phylogeny, still the only known niche subspecialization for S. pneumoniae to date, is critical to understanding the pathogenesis of ocular surface infections, nature of host-pathogen interactions, and developing strategies to curb disease transmission.

Highlights

  • The study of biogeography is primarily concerned with understanding how ecological and geographical forces shape spatial distributions of life in our natural world [1,2]

  • More contemporaneous renderings of microbial biogeography have used models of community ecology in an attempt to explain the processes underlying all microbial assemblage [1,2,4]. Such models point to four fundamental and synergistic principles, which shape all patterns of life in the natural world: selection, diversification, dispersion and ecological drift, which operate on a multiplicity of spatial and temporal scales

  • One of the best examples of the importance of biogeography for human pathogens comes from the evolution of a highly specialized clade of nonencapsulated Streptococcus pneumoniae—the epidemic conjunctivitis cluster (ECC)—which has a near exclusive predilection to infect the conjunctiva [10]. We explore this unique specialization through the lens of biogeography and community ecology, with a focus on new insights regarding the molecular epidemiology of this rogue S. pneumoniae clade which enabled it to become a leading cause of epidemic bacterial conjunctivitis

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Summary

Introduction

The study of biogeography is primarily concerned with understanding how ecological and geographical forces shape spatial distributions of life in our natural world [1,2]. The notion of biogeography was touched on in the now-canonized words of Dutch scientist Lourens Baas-Becking, who in 1934 wrote, “everything is everywhere, but the environment selects” [3] This statement includes two keys as to why microorganisms colonize in the patterns we observe: opportunity or access, and selection for fitness in that habitat. More contemporaneous renderings of microbial biogeography have used models of community ecology in an attempt to explain the processes underlying all microbial assemblage [1,2,4] Such models point to four fundamental and synergistic principles, which shape all patterns of life in the natural world: selection, diversification, dispersion and ecological (stochastic, i.e., random) drift, which operate on a multiplicity of spatial and temporal scales. We offer critical and perhaps generalizable insight regarding fundamental questions of disease pathogenesis, acquisition of virulence factors and the nature of host–pathogen interactions, which are key to the study of all microbiology

Towards a Unified Model of Community Assembly
The Four Tenets of Vellend’s Model
Anatomical Biogeography
Streptococcus pneumoniae
A New Biogeography
Dispersion and Transmission of ECC
Changes in Community Composition Following Human Intervention
Findings
Conclusions
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