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Chapter 18 : Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla

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Abstract:

In recent decades, microbiologists have discovered an astounding disparity of prokaryotic life. Our field has identified the most anciently divergent prokaryotic lineages, and we have found them to be utterly different in every aspect of their being: their cell architecture, biochemistry, physiology, genome content, and how they make a living. Our understanding of the prokaryotes’ phylogenetic diversity began in large part with Carl Woese’s tree of all life, based on the universal 16S rRNA gene ( ). His universal tree yielded the surprising result that the not-yet-named archaea and bacteria, already known to be extremely different in cell structure, represented the deepest divisions of life. Subsequent surveys of 16S diversity, using cultivation-free methods, led to discovery of vast numbers of uncultivated prokaryotic taxa, at all levels from species to phyla, in even the most familiar of habitats ( ). While cultivation has yielded discovery of ∼30 bacterial phyla, cultivation-free methods focusing on 16S have expanded the number of bacterial phyla to nearly 100 ( ). Moreover, we can extrapolate that among rare, presently uncultivable organisms, we will eventually discover ∼1,300 phyla ( )! Most recently, single-cell genomic approaches have yielded much greater resolution for prokaryotic phylogeny and have revealed a totally unexpected superphylum at the base of the bacteria tree. This group is predominated by phyla with limited metabolic capabilities and a shared stubbornness against cultivation ( ). These are all exciting forays into estimating the vastness and organization of prokaryotic diversity, but these purely phylogenetic approaches fail to portray the profound distinctness among the most anciently divergent prokaryotes.

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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Figure 1

Ecological divergence between ecotypes and ecological homogeneity within ecotypes. The ecological divergence between ecotypes is sufficient for them to coexist into the indefinite future. Ecotypes are defined so that any ecological differences among lineages within ecotypes are not sufficient to allow them to coexist indefinitely. We may thus refer to ecologically distinct lineages within ecotypes as “ephemeral ecotypes.” The different styles of dashed lines within ecotype 1 refer to different ephemeral ecotypes; note that only one of these lineages persists to the present. The different weights of solid lines represent different ephemeral ecotypes within ecotype 2 ( ). Used with permission from Elsevier.

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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Figure 2

The consequences of fitness trade-offs in ecological diversification. Improvement of an ecological function by mutation or HGT (indicated by the enlarged triangle) can lead to a periodic selection event (A) or an ecotype formation event (B or C). Each individual is represented by a circle, and each individual’s degree of adaptation to two resources (or conditions) is indicated by the sizes of the square and triangle, respectively. In panel A, adaptation to the triangle resource or condition is increased in one individual (indicated by increased triangle size), and the resultant strain is now able to outcompete the membership of its ecotype by virtue of its more generalist ecology. In panel B, the increase in adaptation to the triangle resource intrinsically decreases the adaptation to the square resource. Thus, increase in one ecological capability comes at the expense of a preexisting capability. In this case, acquisition of the new function leads to a new ecotype, which can coexist with the preexisting ecotype. This has been seen repeatedly in experimental populations of that primarily used glucose for carbon; a mutation to utilize secreted acetate created a new ecotype because the acetate-utilizing bacteria were less able to utilize glucose ( ). An alternative possibility is shown in panel C, where there is no intrinsic trade-off to the new adaptation yet a new ecotype can form. Here the new genotype invades a new habitat where the new adaptation is selected for. If the “square” adaptation is not utilized in one habitat and the “triangle” adaptation is not utilized in the other, under the Black Queen hypothesis, the unnecessary adaptations may be lost ( ). This will make each ecotype the superior competitor in its own microhabitat. Adapted with permission from reference .

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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Figure 3

Models of bacterial speciation. Ecotypes are represented by different colors, periodic selection events are indicated by asterisks, and extinct lineages are represented by dashed lines. The letters at the top represent the resources that each group of organisms can utilize. In cases where ecotypes utilize the same set of resources but in different proportions, the predominant resource of each ecotype is noted by a capital letter. (A) The stable ecotype model. In the stable ecotype model, each ecotype endures many periodic selection events during its long lifetime. The stable ecotype model generally yields a one-to-one correspondence between ecotypes and sequence clusters because ecotypes are formed at a low rate. The ecotypes are able to coexist indefinitely because each has a resource not shared with the others. (B) The speedy speciation model. This model is much like the stable ecotype model, except that speciation occurs so rapidly that most newly divergent ecotypes cannot be detected as sequence clusters in multilocus analyses. (C) The nano-niche model of bacterial speciation. In the figure, there are three nano-niche ecotypes that use the same set of resources but in different proportions (noted by Abc, aBc, and abC). Each nano-niche ecotype can coexist with the other two because they have partitioned their resources, at least quantitatively. However, because the ecotypes share all their resources, each is vulnerable to a possible speciation-quashing mutation that may arise in the other ecotypes. (D) The species-less model. Here the diversity within an ecotype is limited not by periodic selection but instead by the short time from the ecotype’s invention as a single mutant until its extinction. The origination and extinction of each ecotype is indicated by and , respectively. In the absence of periodic selection, each extant ecotype that has given rise to another ecotype is a paraphyletic group, and each recent ecotype that has not yet given rise to another ecotype is monophyletic ( ). (E) Recurrent niche invasion model. Here a lineage may move, frequently and recurrently, from one ecotype to another, usually by acquisition and loss of niche-determining plasmids. Red lines indicate the times in which a lineage is in the plasmid-containing ecotype; blue lines indicate the times when the lineage is in the plasmid-absent ecotype. Periodic selection events within one ecotype extinguish only the lineages of the same ecotype. For example, in the most ancient periodic selection event shown, which is in the plasmid-absent (blue) ecotype, only the lineages missing the plasmid at the time of periodic selection are extinguished, while the plasmid-containing lineages (red) persist. Ecotypes determined by a plasmid are not likely to be discoverable as sequence clusters. Reproduced from reference ( ).

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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Figure 4

The dynamics of ecotype formation and periodic selection within an ecotype. Circles represent different genotypes, and asterisks represent adaptive mutations. (A) Ecotype formation event. A mutation or a recombination event allows the cell to occupy a new ecological niche, founding a new ecotype. A new ecotype can be formed only if the founding organism has undergone a fitness trade-off, whereby it cannot compete successfully with the parental ecotype in the old. (B) Periodic selection event. A periodic selection mutation improves the fitness of an individual such that the mutant and its descendants outcompete all other cells within the ecotype; these mutations do not affect the diversity within other ecotypes because ecological differences between ecotypes prevent direct competition. Periodic selection leads to the distinctness of ecotypes by purging the divergence within but not between ecotypes. Reproduced with permission from reference .

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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Figure 5

Genome-wide and single-chromosomal-region sweeps within a sequence cluster of closely related bacteria. Each row of panels represents a different model of sweep within a metagenome cluster: (A to B) a genome-wide sweep, where the metagenome cluster is populated by only a single ecotype, and where recombination is rare enough to allow a genome-wide sweep within an ecotype ( ); (C to D) a narrow sweep (homogenizing only the chromosomal region near the adaptive mutation), where again the metagenome cluster is populated by a single ecotype, but here recombination (indicated by purple arrows) is frequent enough to prevent a genome-wide sweep within an ecotype (model favored by Bendall et al. [ ]); and (E to H) a narrow sweep, where the metagenome cluster is populated by many ecotypes (in this case, three), and recombination is rare enough to allow genome-wide sweeps within an ecotype but frequent enough to allow an adaptive mutation to recombine (it need happen only once!) between one ecotype and another ( ). In each row, the wide horizontal arrows represent the course of time. In each panel, the rectangle represents one metagenome cluster and each circle represents a single organism. The asterisk represents an adaptive mutation, which allows its carrier to outcompete other organisms in the same ecotype but not organisms from other ecotypes. In panels A to D, the metagenome cluster is ecologically homogeneous, and in panels E to H, the metagenome cluster is ecologically heterogeneous and represents three ecotypes, separated by the vertical dashed lines; the different ecotypes are coded by blue, green, and red. The sequence diversity within an ecotype is represented by different shades of the ecotype color and by different styles of line (dotted, dashed, and solid). In the case of low recombination rates (A to B and E to H), the adaptive mutation causes a genome-wide sweep within the ecotype containing the mutation. In panels E to H, the adaptive mutation is potentially beneficial in different ecotypes and can transfer on a short chromosomal segment to another ecotype, where it precipitates a new genome-wide sweep within its new ecotype. Reproduced with permission from reference ( ).

Citation: Cohan F. 2019. Transmission in the Origins of Bacterial Diversity, From Ecotypes to Phyla, p 311-343. In Baquero F, Bouza E, Gutiérrez-Fuentes J, Coque T (ed), Microbial Transmission. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MTBP-0014-2016
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