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Greenspan, A. Photosynthetic Cyanobacteria: Are They the Only?

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Greenspan, A. Photosynthetic Cyanobacteria: Are They the Only? Photosynthetic Cyanobacteria: Are they the only? Alex Greenspan UC Davis Microbial Diversity 2012 Abstract: The advent of oxygenic photosynthesis marks one of the singularly most important events in life's history. However, the origins of oxygenic photosynthesis are poorly understood. All known oxygenic photosynthesis is performed by members of the bacterial phylum cyanobacteria and all cultivated cyanobacteria are capable of oxygenic photosynthesis. Since the advent of 16S rRNA sequencing for in situ identification of microbes in their environments, various environmental surveys have yielded 16S sequences which group on the cyanobacterial branch of bacterial phylogeny, basal to any known photosynthetic cyanobacteria. Based on the environmental distribution of the different clusters of these basal cyanobacterial sequences, many of these speculative groups seem to grow obligately in the dark, suggesting that some of these sequences may belong to extant, ancestral, aphotic cyanobacteria. The discovery and isolation of such organisms would likely yield invaluable information about the origins of oxygenic photosynthesis. This project was directed at further characterizing these organisms based on their phylogeny and observed environmental distribution to contribute towards further attempts at isolating ancestral, aphotic cyanobacteria. In addition to phylogenetic analysis, I also attempted to design PCR primers specific for the environmental groups, which would greatly aid any later attempts at enriching and isolating these organisms. Background: The ability to fix carbon from light energy is distributed through a diverse selection of bacterial groups, and involves a similarly wide variety of chemistries (Overmann and Garcia-Pichel, 2006). Different organisms have evolved to utilize different wavelengths of light to transfer electrons from a variety of electron donors ultimately to carbon dioxide. Of those capable of photosynthesis, only one group of related organisms have evolved to utilize water as an electron donor, resulting in the production of molecular oxygen: the cyanobacteria. The advent of this process almost certainly marked the shift in the Earth from an anoxic to oxic atmosphere. The consequences of this event on the trajectory of life's evolution are incomparable. All known cyanobacteria today are capable of oxygenic photosynthesis. However, given the patchy distribution of photosynthesis in the nearest-related groups of bacteria to cyanobacteria, it is unlikely that their last common ancestor was photosynthetic (for more on this claim, and really greater details on all of the biochemistry and phylogeny of photosynthesis which I'm somewhat neglecting here, check out James Hemp's 2011 report from the course). Several studies have used comparative genomics to search for clues to the origins of photosynthesis in this group. Mulkidjanian et al. (2006) infer somehow that photosynthesis itself may have originated with the cyanobacteria. Beck et al (2012) manage to infer core metabolic pathways for all cyanobacteria. In any case, if we're interested in how photosynthesis originated in the group, ultimately what we need is to find out what they were doing before photosynthesis entered the lineage. A diversity of fermentative pathways are widely conserved among a broad range of cyanobacteria (Stal, 1997), so this seems like a plausible ancestral way of life. What we would want to have, in order to truly learn anything about the origins of oxygenic photosynthesis in cyanobacteria, is an isolate representing aphotic, ancestral cyanobacteria. We have reasons to believe such an organism might exist. Numerous 16S rRNA gene sequencing surveys have identified sequences which group at the base of the cyanobacterial branch of the tree of life. Many of these sequences seem to come from conserved clades that are consistently found in analogous environments, and many of these environments are consistently dark (for example, many sequences from a seemingly monophyletic group have been found in the guts of a surprising array of animals. More on this in a moment). For a good review of these sequences, see Ruth Ley's paper on mouse gut microbiota (2006). This report is an attempt both to better characterize these groups phylogenetic and environmental distribution, as well as to develop methods for rapidly quantifying these potential basal cyanobacteria in enrichments. Results and Discussion: Phylogenetic Analysis: The most plausible candidates for ancestral, aphotic cyanobacteria are those organisms—which have been detected by environmental 16S rRNA gene sequencing surveys—whose 16S rRNA gene sequences fall low (basal to photosynthetic cyanobacteria) on the cyanobacterial branch of bacterial phylogenies. The most extensive and interactive source for exploring environmental 16S sequences in the context of overall bacterial diversity is the Silva Arb database. In the most recent non-redundant Silva Arb database, 108, there are 7 groups of sequences which fall on the cyanobacterial branch of the bacterial tree, basal to all known photosynthetic cyanobacteria but above the root of the branch where cyanobacteria split from their nearest neighbors. If organisms related to ancestral cyanobacteria exist today, it is likely those that possess these sequences. The Silva Arb database is constructed by using the parsimony insertion tool in Arb to add curated, aligned sequences (above a certain alignment quality) a guide tree inferred de novo from sequences in the previous release. The parsimony insertion algorithm, while powerful and invaluable for identifying previously unknown sources of microbial diversity, is not especially sensitive in resolving deeply divergent branchings and gives no estimate of the confidence in any given grouping. In order to resolve the relation of putative ancestral cyanobacterial lineages to known cyanobacteria, I constructed a phylogenetic tree of 16S rRNA sequences representing known, photosynthetic cyanobacteria, all the putative basal clades, as well as representatives of cyanobacterias' nearest neighbors in the bacterial tree (Figure 1). Phylogenetic analysis served to answer three primary questions about the putative basal cyanobacterial groups. A cursory examination of the basal cyanobacterial clades in the Silva Arb tree reveals a relationship between environment and phylogeny among the groups; most sequences that cluster together into basal clades in the cyanobacteria branch in Arb were extracted from the same environment, and most sequences extracted from certain environments in the cyanobacteria tree will fall into the same group. For example sequences that fall into the group labeled 4c0d in the Figure 1: Maximum likelihood phylogenetic tree of representatives of photosynthetic cyanobacteria, putative basal cyanobacteria, and cyanobacteria nearest neighbors, using Beggiatoa alba as an outgroup. Branches are colored by phylogeny. Leaves are colored by environment the sequences were derived from. cyanobacteria branch in Arb were found predominantly in 16S surveys of animal guts or animal feces, and most of the cyanobacterial sequences derived from guts are found in the 4c0d branch (with the exception of the SHA-109 group, which contains many sequences from a single survey of sheep rumen). Furthermore, the gut-associated sequences in 4c0d were derived from numerous independent investigations or different guts and surprisingly wide diversity of feces (orangutan, elephant, penguin, zebra, mouse, etc). Similarly, the group MLE1-12 has been observed primarily in drinking water and drinking water associated habitats (e.g. drinking-water treatment plants, aquifers, etc). Surprisingly, MLE1-12 does not contain many sequences from other fresh-water habitats (e.g. lakes, rivers), but seems almost solely to have been observed in below-ground, human associated water sources. The first question I wanted to answer about these basal cyanobacterial sequences was whether these environmental associations hold up to more rigorous phylogenetic analysis. This question can be addressed somewhat through bootstrapping: a technique whereby positions sequences in an alignment used to build a phylogenetic tree are randomly resampled with replacement, trees are reconstructed from the random resamples, and clades are scored based on whether all of the members of that group based on the consensus tree are present in a given bootstrap tree; a bootstrap value of 70 on a given node means that all leaves above that node were present above that node in 70 percent of the randomly generated trees but does not tell you which sequences moved nor where they moved in the other 30 percent of the bootstrap trees. This gives you some measure of confidence that there is sufficient phylogenetic signal in the sequences to infer accurate relationships. Anyway, getting back to the tree. Three of the original basal cyanobacterial groups in the Silva tree end up on the cyanobacterial branch (above the split with the neighboring groups). Two of these groups (the gut group 4c0d and the drinking water group MLE1-12) have very high bootstrap support (97 and 98 % respectively). The remaining group (ML635J21) splits into two groups which cluster by environment (soil and marine sediment), of which the sediment group is well supported (bootstrap=99). Figure 2: Maximum likelihood tree of cyanobacteria and nearest neighbors after removing low quality sequences and clustering basal groups Likewise, the remaining putative basal cyanobacterial groups have reasonably high
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