The Rare Biosphere

One might think that the age of great discoveries in biology is past––that humans have been everywhere and seen everything on Earth. But in fact, biology still boasts some formidable unknowns, and many are now being explored in the once invisible world of microbes. In the last 20 years, technological advances have made it possible to explore a microbial world that has proven vastly more extensive, important, and diverse than previously imagined. Analyses of microbial communities in the soil, in the ocean, and even in the human body, have shown that previous methods detected only a tiny percentage of the different microbes in these environments. It seems that each technological advance and every new environment sampled reveal even greater diversity in the microbial world. Is there a limit? How can the nature and extent of microbial diversity be satisfactorily characterized? On a more fundamental level, how did evolution generate such diversity, how is it maintained, and what are its practical implications?

Molecular methods for analyzing microbial communities suggest that in addition to a few abundant microorganisms, which can exist at concentrations of thousands or even millions per liter of water or gram of sediment, nearly all microbial communities include many members that are rare. Thus, microbial communities are like libraries that contain hundreds of copies of a few books and a single copy each of thousands of others. In some cases, the rare groups in microbial communities can, collectively, comprise up to 75% of the biomass in their communities, and the total number of genomes represented in this fraction is potentially huge. An emerging term for these groups is “the rare biosphere”.

In April, 2009, the American Academy for Microbiology convened a colloquium in San Francisco, California to review the current state of research on the rare biosphere and describe knowledge gaps on which to focus future work to move our understanding of these taxa forward. This document summarizes those discussions.

Indeed, much remains to be learned about the rare biosphere. It is not known, for example, whether there are some groups that are always rare, in every environment—in other words, groups for which “rareness” is an evolutionarily conserved way of life. Whether the rare groups are transient or persistent in any given community also is not clear. Some groups that are rare in one environment may be abundant in others, or groups that are rare under certain conditions may become abundant when conditions change. These open questions suggest that defining particular groups as “rare” and others as “non-rare” will be context-dependent.

The number of different habitats in which microbial assemblages are found is vast; not only does every environment––sea, soil, building surface, even cloud––host a variety of different microbial communities, so does every animal and plant. If, as is likely, the rare biosphere is made up of different groups in each of these habitats, it represents a truly staggering potential reservoir of genetic diversity.

Humans are host to many different microbial communities that live on our skin, in our guts, in our mouths and elsewhere. Collectively called the human microbiome––these microbial communities are increasingly being shown to be critical to human health and well-being. Thus, in addition to roles the rare biosphere may play in the environment, further study of the rare biosphere portion of the human microbiome could provide insights into such issues as hygiene theory, infections in infancy, gut methanogenesis, and the impacts of commensal diversity on human health and disease.

The consistent detection of a large number of rare groups in most microbial assemblages could have significant fundamental and practical implications and suggests that they have a role to play in microbial community dynamics. They may carry out keystone physiological functions, maintain community-level function in the face of environmental change, or serve as a reservoir of genetic resources that can provide novel material to the community as needed.

The most appropriate spatial and temporal scales for exploring the dynamics and functional role of the rare biosphere will vary for different habitats. Appropriate specific experimental strategies will be required to explore microbial diversity in all potential habitats, but in general, more intensive, or “deep” sequencing than is typical of microbial community analysis, and repeated sampling over time will likely be needed in order to better capture community dynamics and explore the temporal stability of the rare biosphere.

To address these questions research should focus on the spatial and temporal distribution of rare taxa, their functional and ecological roles, and evolutionary mechanisms that maintain a rare biosphere of highly diverse, low abundance microbial populations. These investigations must also assess how varying sampling and extraction techniques might affect our understanding of the rare biosphere.