Rare biosphere

Changes in the biodiversity of an ecosystem, whether marine or terrestrial, may affect its efficiency and function (Gitay et al., 2002). Disruption due to climate change, or other anthropogenic perturbations, can result in decreased productivity and in some cases lead to disruptions in global biogeochemical cycles (Gitay et al., 2002). It is important to note that the possible ramifications of changes in ecosystem biodiversity are not well characterized or understood, and it may be possible that disruption, up to a point, will have little to no affect given the redundancy within an ecosystem (Gitay et al., 2002). This is particularly troubling in the context of microbial ecosystems. The dynamics of microbial ecosystems are tightly coupled to biogeochemical processes, and any perturbation within this system in particular could result in dramatic changes (Kirchman, 2008). For example, the microbial loop within the marine context is responsible for the decomposition of organics and recycling of nutrients back into the ecosystem. This allows for other organisms, such as phytoplankton, to reuse essential nutrients, like nitrogen, and continue production (Kirchman 2008). Without this recycled nitrogen phytoplankton would be highly limited in their production rates, in turn limiting the growth of grazers. The effects of such an occurrence would reverberate throughout the food web, and nitrogen cycle. It is important to establish a base line of microbial diversity within ecosystems in order to gauge possible change due to climate change and the possible outcomes.

Recent use of high throughput sequencing techniques has broadened the scope of biodiversity, with the discovery of what has been titled the “Rare Biosphere” (Sogin et al., 2006). Previous attempts to characterize in situ abundance have been made through pure culture and molecular techniques (Fuhrman, 2009). Pure culture providing a very narrow picture of some of the more rare species present, <1-5% of bacteria present (Fuhrman, 2009). Molecular techniques, such as Sanger sequencing, resulting in a much broader scope but highlighting the more abundant species present (Heidelberg et al., 2010)(Pedros-Alio, 2007). Neither technique captures all of the diversity present. Alternatively high throughput sequencing, “tag sequencing”, divides unique rRNA tag sequences into operational taxonomic units (OTU’s) based upon similarities in mitochondrial-encoded cytochrome oxidases (Sogin et al., 2006). Both Sanger, shot gun sequencing, and tag sequencing organize sequences into OTU’s (Heidelberg et al., 2010). However, it is the resolution that tag sequencing provides that sets it a part, resulting from the increased efficiency in serial analysis (Heidelberg et al., 2010). This efficiency increase is made possible through the use of internal primer sequences resulting in restriction-digest overhanging sequences (Heidelberg et al., 2010). Though OTU’s provide a means of distinguishing the possible number of phylogenetic groups, it is not possible to deduce phylogenetic relationships based upon OTU’s. Tags associated with OTU’s must be cross referenced with gene banks, in order for tags to be phylotyped and relationships established (Sogin et al., 2006).

The result of tag sequencing has been to produce orders of magnitude larger estimates of OTU’s present in ecosystems, producing a long tail on species abundance curves (Patterson, 2009)(Pedrós-Alío, 2007). This long tail accounts for less than .1% of the abundant species in a particular ecosystem. At the same time it represents thousands of populations accounting for most of the phylogenetic diversity in an ecosystem. This low abundance high diversity group is what is now called the “Rare Biosphere”. Using this method Sogin et al.’s study of microbial diversity in North Atlantic deep water produced an estimate of 5266 different taxa (Sogin et al., 2006). This is particularly dramatic considering that previous studies employing more traditional PCR cloning techniques have resulted in estimates of up to 500 (Pedrós-Alío, 2007).

Ecological Role

Marine Context

Considering their low abundance, members of the rare biosphere may represent ancient and persistent taxa (Sogin et al., 2006). As these less abundant species are limited in number viral infection, and ultimately death by lysis, is unlikely (Pedrós-Alío, 2007). Viruses depend on high concentrations of hosts to persist. Additionally being less abundant implies limited growth, and on the smaller end of the cell size spectrum (Pedrós-Alío, 2007). This limits the likelihood of death by ingestion, as grazers prefer larger more active microbes. As well it is important to note that just because these taxa are “rare” now does not mean that under previous conditions in our planet’s history they were “rare” (Sogin et al., 2006). These taxa could be have been episodically abundant, resulting in global changes in biogeochemical cycles (Sogin et al., 2006). Essentially this requires microbial ecologists to change their perspective on how microbial interactions function on evolutionary time scales (Sogin et al., 2006).

On that note, rare today does not mean rare tomorrow. Given the persistence of these taxa under the right conditions they have the potential to dominate, and become the more abundant taxa (Sogin et al., 2006). The occurrence of such conditions may occur on many temporal scales. It may be possible that some rare taxa dominate only during anomalous years, such as during El Niño (Fuhrman, 2009). While, a four-year study by Brown et al. in species abundance in a single marine ecosystem found that some taxa were undetectable during some months and accounted for a couple percent of the total abundance other months (Brown et al., 2009). Indicating that a change in abundance may occur on a seasonal scale. Recent global climate change may provide some of these rare taxa with the conditions necessary to increase in abundance. Even in their low abundance taxa belonging to the “Rare Biosphere” may be affecting global biogeochemical cycles. For example, most of nitrogen fixation was attributed to Trichodesmium and abundant cyanobacterium. However, more recent evidence implicates that the rare minority may be responsible for fixing more cumulative Nitrogen than the abundant majority (Furhman, 2009).

A subtle and less direct manner these populations may be affecting ecosystems, in terms of biodiversity and biogeochemical cycles, is by acting as an unlimited source of genetic diversity and material (Furhman, 2009)(Sogin et al., 2006). How microbial communities present resilience after environmental perturbation or catastrophe and how closely a closely related species may present unique and novel genetic attributes compared to near relatives, are topics of much discussion and investigation (Sogin et al., 2006). The rare biosphere could be a seed bank, transferring genes resulting in fitter recombinants that rise to become the dominant majority (Sogin et al., 2006). Until now this group has been overlooked entirely, and may be the answer to many longstanding questions concerning microbial ecology and genetics.

Biogeography and Distribution

Marine Context

There is some debate concerning the distribution of taxa within the “Rare Biosphere”. Taxa within this group at a given site may be in the process of dispersal (Fuhrman, 2009)(Patterson, 2009). Studies in the Arctic seabed identified thermophilic bacteria, arriving through mechanisms of dispersal, that could not be metabolically active (Patterson, 2009). Once these populations, such as the thermophilic bacteria in the Arctic, reach a suitable niche they will again become metabolically active and increase in abundance. This requires that one view these populations as non-discrete, not endemic to any one particular body of water (Patterson, 2009). Rather view populations as continuous throughout the oceans. Alternatively, studies suggest that given the biogeography of rare taxa the idea of the rare biosphere being the product of dispersal seems unlikely (Galand et al., 2009). Galand et al. completed a study in the Arctic Ocean on the biogeography of the rare biosphere and found that between parcels of water within that ocean the rare biosphere presented a large amount of diversity (Galand et al., 2009). Suggesting that populations within the rare biosphere experience evolutionary forces specific to the location they are found such as selection, speciation, and extinction (Galand et al., 2009). Asserting that water masses have physical boundaries resulting in highly evolved and divergent taxa between rare biospheres from different locations (Galand et al., 2009). Also, given the fact that many rare taxa cannot be identified in gene banks, it seems unlikely that they abundant elsewhere (Galand et al., 2009). Though this statement is difficult to validate, due to the extreme under sampling of marine ecosystems (Heidelberg et al., 2010).

References

• Brown, M. V., Schwalbach, M. S., Hewson, I. & Fuhrman, J. A. Coupling 16S-ITS rDNA clone libraries and ARISA to show marine microbial diversity: development and application to a time series. Environ. Microbiol. 68, 1015-1024 (2002).
• Fuhrman, Jed A. "Microbial Community Structure and Its Functional Implications." Nature 459.7244 (2009): 193-99.
• Galand, Pierre E., Emilio O. Casamayor, David L. Kirchman, and Connie Lovejoy. "Ecology of the Rare Microbial Biosphere of the Arctic Ocean." PNAS 106.52 (2009): 22427-2432.
• Gitay, Habiba. Climate Change and Biodiversity. [Geneva, Switzerland?]: Intergovernmental Panel on Climate Change, 2002.
• Kirchman, David L. Microbial Ecology of the Oceans. Hoboken, NJ: Wiley-Blackwell, 2008. Print.
• Patterson, D. J. "Seeing the Big Picture on Microbe Distribution." Science 325.5947 (2009): 1506-507.
• Pedrós-Alío, C. "ECOLOGY: Dipping into the Rare Biosphere." Science 315.5809 (2007): 192-93.
• Sogin, M. L., H. G. Morrison, J. A. Huber, D. M. Welch, S. M. Huse, P. R. Neal, J. M. Arrieta, and G. J. Herndl. "Microbial Diversity in the Deep Sea and the Underexplored "rare Biosphere"" Proceedings of the National Academy of Sciences 103.32 (2006): 12115-2120. open access link