Microbial Evolution and Co-Adaptation A Tribute to the Life and Scientific Legacies of Joshua Lederberg: Workshop Summary (2009) / Chapter Skim
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2 Microbial Ecology and Ecosystems
2 Microbial Ecology and Ecosystems
Pages 95-120
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From page 95... ...
From the RNA sequences of the microbiome (a term coined by Lederberg to encompass the collective genome of organisms living in and on the human body) , Relman and colleagues infer the diversity of organisms present in various indigenous microbial communities and compare patterns of ancestry and relatedness among these communities, between individual humans, and with those of microbial communities inhabiting external environments.
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From page 96... ...
Focusing on interactions within communities of microbes, speaker Jill Banfield, of the University of California, Berkeley, described research conducted in her laboratory to elucidate the structure, function, and development of biofilms, and on the role that viruses play in these communities. These inquiries, she said, pose the following questions: "How do activities of organisms change as microbial communities establish?
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From page 97... ...
Thus, Banfield concluded, there appeared to be strong local selection for this particular genotype, which has "achieved a fine level of adaptation to environmental opportunity." Turning to the role of viruses in biofilms, Banfield noted that the host specificity of viruses, coupled with their generally negative host effects, suggests that viruses profoundly and dynamically shape the membership of microbial communities. Focusing on the viral "predators" of the dominant bacterial species in biofilms, her laboratory was inspired by recent reports (Makarova et al., 2006; Mojica et al., 2005)
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From page 98... ...
"The virus maintains a high population diversity so the host immune system cannot silence it," Banfield explained. "This would, in itself, make the task of the host, the CRISPR loci, rather difficult." However, she added, there is also considerable diversity in the host genome, where they found "incredible heterogeneity, to the point that we would deduce that almost no two cells within a microbial community are the same." Thus, while a "cloud of viruses" maintains high levels of sequence diversity by various means in order to defeat host microbes within the biofilm, the viruses are countered by the rapid acquisition of new viral spacers by the microbes.
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From page 99... ...
In the meantime, the discovery that a largely shared signaling pathway makes possible both arbuscular mycorrhization and legume nodulation -- despite their apparent differences -- has led to the conclusion that plants have a single, highly conserved genetic program for recognizing beneficial microbes, according to Ané. Both microbial Nod and Myc factors also appear to have common features, including the ability to promote plant growth.
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From page 100... ...
In the chapter's final paper, speaker Margaret McFall-Ngai of the University of Wisconsin explores the question, "What are the shared characteristics of pathogenic and mutualistic interactions between microbes and their animal hosts? " She pursues this by studying a model system: the association formed between the Hawaiian bobtail squid, Euprymna scolopes, and the gram-negative luminous bacterium Vibrio fischeri, which populates the squid's light organ.
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From page 101... ...
A major purpose of exploring the human microbiome is to understand the role of indigenous microbial communities in human health and disease -- and the various transition states between them. By understanding essential features of symbiotic relationships between microbial communities and their human host -- a difficult task from a practical point of view -- it may eventually be possible to predict host phenotypes, such as health status, from the particular features of indigenous communities.
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From page 102... ...
We are not yet able to perform the kinds of precise manipulations of the human microbiota that can be undertaken with simpler microbial communities and model systems, so -- as I will subsequently describe -- we have chosen to look at natural and clinically relevant forms of perturbation to understand the performance features of these communities. Patterns of Diversity The diversity of the human microbiome can be inferred from its collection of microbial ribosomal RNA sequences.
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From page 103... ...
. Why are so few phyla found on or within the human body?
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From page 104... ...
By the end of the first year of life, the distinct microbiota of each baby had converged toward a profile characteristic of a generic adult gastrointestinal tract. The studies that I have discussed so far, along with others, reveal features of human indigenous microbial diversity that deserve further study: the same few
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From page 105... ...
; limited archaeal diversity; individuality and host-specificity; and the importance of early events and exposures in establishing that individuality. There are multiple possible sources of variation and variability in the indigenous microbiota, including host genetics, local anatomy, pH, oxygen concentration, age, diet, place of birth and residence, occupation, contacts with other humans and animals, and perturbations such as antibiotic treatment or mechanical disruption.
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From page 106... ...
(B) Vertebrate-associated habitats have few deep lineages but each displays a broad radiation bitmap images of shallow lineages.
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From page 107... ...
The detrimental consequences have yet to be fully appreciated, but include acute disease, chronic disease, and emerging resistance. In my laboratory, Les Dethlefsen has been examining the effects of antibiotics on the distal gut microbiota in healthy subjects, in order to determine how patterns of diversity vary before, during, and after these exposures, and to assess community resilience.
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From page 108... ...
Focusing on a particular genus, the Bacteroides, we found that during and just after the ciprofloxacin exposure, there was a rise and fall in species abundance in all three individuals, as shown in Figure 2-5. However, although there was not FIGURE 2-5 Individualized responses to the same antibiotic: Abundance of 16S rRNA Figure 2-5 COLOR.eps V3 sequence tags corresponding to Bacteroides species -- before and after ciprofloxacin administration (gray shaded zone corresponds image bitmap to sampling times during or immediately after administration)
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From page 109... ...
Second, we also need to understand better how and where to sample microbial communities within the human body. In particular, we need to determine the spatial scale within each human habitat at which clinically and ecologically relevant distinctions in microbial diversity found.
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From page 110... ...
Specifically, is the language of these different types of associations controlled principally by different cellular and molecular characters wherein divergent genes and pathways are used to mediate bacterial activity and host responses (i.e., are they "polyglot") ; or by shared mechanisms in which the outcome is determined by when and where identical molecules and pathways are brought into play (i.e., are they Esperanto3-like)
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From page 111... ...
How will this newfound knowledge affect our view of the biology of pathogenic associations and how pathogenesis should be treated in clinical settings? In a broader view, it is now becoming clear not only that the microbial communities associated with host animals affect the tissues with which they interact but also that their metabolic products interact with most cells of the body (Nicholson et al., 2004)
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From page 112... ...
. From that milestone in evolution, the association of microbes with the apical surfaces of host epithelia, whether they are mutualistic, commensal, or pathogenic, has been the dominant type of animal-microbe relationship.
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From page 113... ...
However, when V fischeri cells are present, they exert competitive dominance in the mucus, such that by 2-3 hours following exposure to natural seawater, which contains ~106 nonspecific bacteria per milliliter with only a few hundred symbionts, most of the cells in the mucus aggregates are symbiont cells.
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From page 114... ...
The window in the center illustrates the position of the light organ (the green confocal image) image bitmap in the middle of the mantle (body)
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From page 115... ...
of the juvenile light organ that
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From page 116... ...
These host and symbiont resources have paved the way for characterization of the various phases of the symbiosis with an hour-by-hour resolution. The first array experiments of host responses were carried out at 18 hours following initial exposure to the symbiont (Chun et al., 2008)
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From page 117... ...
We anticipate that this study will provide insight into how animals maintain symbioses stably over their life cycle. Summary: The Esperanto of Symbiosis Research on the squid-vibrio symbiosis has demonstrated that both the host and symbiont signal one another with a biochemical, molecular, and cellular language that is typically associated with mediating bacterial pathogenesis of animal tissues.
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From page 118... ...
2008. Virus population dynamics and acquired virus resistance in natural microbial communities.
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From page 119... ...
2008. Explor ing microbial diversity and taxonomy using SSU rRNA hypervariable tag sequencing.
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From page 120... ...
Gnotobiotic zebrafish reveal evolutionarily conserved responses to the gut microbiota. Proceedings of the National Academy of Sciences 101(13)
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