Microbial Diversity Revisited

I have posted on microbial diversity in the soil previously. Tara pointed out that even though we are just now learning about what ecological factors determine soil microbial diversity, we also have a lot to learn about microbial diversity within the human digestive tract. She asked:

I wonder what a meta-analysis of the diversity of human-associated bacteria would find? For example, we already know that diversity can vary even by location within the colon; we also know that the pH of different areas in the body can vary (due not only to bodily secretions but also other bacterial flora that may be present). How much is this a factor in the diversity in our own normal flora?

For those interested in learning more about intestinal microbes, here is a review of the human intestinal symbionts and parasites (subscription required). I'm sure most of it is old hat to Tara, but I'm not all that familiar with this stuff, so it was an interesting read. I have reproduced a few choice quotes below the fold.

On what we found within our intestines:

Because we are born germ free, the microbes that populate our intestinal tract must come from the outside. Microbial diversity on our planet is vast: although 55 divisions (deep evolutionary lineages) of Bacteria and 13 divisions of Archaea have been described to date (DeLong et al., 2001; Rappe et al., 2003; Rondon et al., 1999), much diversity remains unexplored. The intestine is remarkable for its exclusivity: selection pressures whittle down the microbial diversity of the outside world so that the gut microbiota in adults is dominated by members of just two divisions of bacteria -- the Bacteroidetes and Firmicutes -- and one member of Archaea, Methanobrevibacter smithii (Bäckhed et al., 2005; Eckburg et al., 2005). The gut microbial community presumably has strict requirements for membership: an arsenal of enzymes to utilize available nutrients; cell-surface molecular paraphernalia to attach to the "right" habitat, evade bacteriophages, and appease a reaction-ready immune system; genetic gadgetry for mutability to stay well adapted; the ability to grow rapidly to avoid washout; and the stress resistance needed when making the jump to other hosts via a largely dry and toxic "ex-host" environment.

On the evolutionary relationships of intestinal microbes:

This type of extreme fan-like phylogenetic architecture may be a signature feature of the gut ecosystem. Shallow phylotype fans have been described in other natural habitats (e.g., the ocean [Acinas et al., 2004]), but these habitats appear to harbor a greater number of intermediate-level phylogenetic groups than the gut (Figure 2B). The pattern of phylotype fans in the gut recalls the patterns in classic adaptive radiations (Schuter, 2000), such as the radiation of terrestrial snail species of French Polynesia (Garrett, 1884) where a few successful early colonists gave rise to a variety of descendants. Shallow, wide radiations result from extreme selection pressure followed by détente. In the case of the snails, the selection pressure came in the form of a wide ocean to cross, but once there, the early snails filled an island's worth of empty niches (professions) across a range of habitats (addresses). Similarly, the phylogenetic architecture of the gut could have resulted from the diversification of a discrete limited initial community (a population bottleneck) into strains. In addition, the phylogenetic "shallowness" of the intestinal community reflects the relatively short time that the mammalian gut has existed as a habitat (~100 million years for mammals with placentas [Murphy et al., 2001], versus >3.85 billion years for the ocean).

How the microbes get into our intestines:

Pathogens that use an oral-fecal route for their transmission (e.g., members of the Proteobacteria such as Vibrio cholera) can exploit environmental reservoirs outside of their hosts to proliferate. However, members of the Firmicutes and Bacteroidetes detected in the human gut do not appear to grow outside of their host and likely rely on the close contact of parents and offspring for transmission. One testable prediction of this parent-to-offspring transmission hypothesis is that microbial communities will be similar in members of a given family. In experiments with C57Bl/6 mice, we showed that animals inherited their microbial communities from their mothers (Ley et al., 2005), using the recently developed UniFrac metric (Lozupone et al., 2005). Related mice shared similar bacterial communities: the effect was evident across multiple generations: the mothers that were sisters shared microbiotas with each other as well as with their offspring. These findings demonstrate that a microbiota can be inherited vertically from mothers and is stable enough over time that kinship relationships are reflected in community composition.

Culture-based studies in humans indicate that babies acquire their initial microbiota from the vagina and feces of their mothers (Mandar et al., 1996). Babies delivered by caesarian section have an altered colonization pattern relative to their vaginally-delivered counterparts (Gronlund et al., 1999).

On future directions:

To obtain a more comprehensive view of the microbiome, we have proposed a human gut microbiome initiative (Gordon et al., 2005; HGMI) that will deliver deep draft whole genome sequences for 100 species representing the bacterial divisions known to comprise our distal gut microbiota. We have identified 86 cultured representatives (22%) of the 395 phylotypes identified in the human colon. The deposited curated genome sequences would herald another phase of the "human" genome sequencing project, provide a key point of reference for interpreting "metagenome" sequencing projects that use total microbial community DNA as starting material for shotgun sequencing, serve as a model for future initiatives that seek to characterize our other extraintestinal microbial communities, and facilitate analysis of how selective pressures and community dynamics have shaped the microbiome in diseased humans and in gut pathogens.

There's also some stuff on ecology, but, seeing as I'm no ecologist, I won't delve into it. Long story short, it turns out, we're actually a lot like these guys...

Ley, RE, DA Peterson, JI Gordon. 2006. Ecological and Evolutionary Forces Shaping Microbial Diversity in the Human Intestine. Cell. 124:837-848.


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