Massive genome reduction occurred prior to the origin of coral algal symbionts
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Abstract
Dinoflagellates in the Family Symbiodiniaceae (Order Suessiales) are diverse, predominantly symbiotic lineages that associate with taxa such as corals and jellyfish. Their ancestor is believed to have been free-living, and the establishment of symbiosis (i.e., symbiogenesis) is hypothesised to have occurred multiple times during Symbiodiniaceae evolution. Among Symbiodiniaceae taxa, the genus Effrenium is an early diverging, free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here we present de novo assembled genomes and associated transcriptome data from three isolates of Effrenium voratum . We compared the Effrenium genomes (1.2-1.9 Gbp in size) and gene features with those of 16 Symbiodiniaceae taxa and other outgroup dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. We postulate that adaptation to an extreme habitat (e.g., as in Polarella glacialis ) or life in oligotrophic conditions resulted in the Suessiales ancestor having a haploid genome size < 2Gbp, which was retained (or reduced) among all extant algae in this lineage. Nonetheless, our data reveal that the free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (∼30%) lineage-specific gene families, and lower (∼10%) level of pseudogenisation. These results demonstrate how genome reduction and the adaptation to symbiotic versus free-living lifestyles intersect, and have driven the diversification and genome evolution of Symbiodiniaceae.
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These results suggest that in addition to convergent evolution in the symbiotic lineages, these lineages of Symbiodiniaceae have experienced a greater extent of pseudogenisation than has the free-living Ev.
Again, I would just be cautious in the assumption of convergent evolution here, as this is an alternative hypotheses that has not yet been explicitly tested.
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(A) Number of protein families is shown at each node and branch represents those that are shared among or specific to S1, Ev, S2, and/or Po. Number of families that are exclusive to Ev (green), to S1 (light blue), to Ev+Po (dark blue), to S2+S1 (yellow), and to S2+S1+Po (orange) were highlighted.
This sub-plot would again support an interpretation in which (at least some/many) genes related to a symbiotic life history were gained once in S1, and subsequently lost in Ev.
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Incidentally, Po shared more protein families with symbiotic lineages (1,290; S1+S2+Po) than with Ev (221; Ev+Po);
Okay, this addressed my comment above, but I would say that this supports an interpretation that the large numbers of genes shared between the symbiotic clades arose once in S1, but were subsequently lost in Ev, being retained in S2.
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The high number of protein families present only in symbiotic lineages that split from each other over 40 million years of evolution suggests convergent evolution due to the symbiotic lifestyle.
How exceptional is this count of shared gene families among the two symbiotic lineages? Does it exceed what is shared between only (for instance) Ev and Po, or S1/2 and Po?
I feel that convergence of the gene families shared between the two symbiotic clades is an alternative hypthothesis that should be tested, rather than assumed. An alternative explanation is that these are genes that arose once within S1, and were subsequently lost within Ev.
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The driving mechanism for this trend may reflect one of two evolutionary scenarios: (a) intron expansion in Ev, or (b) intron contraction in S1/S2.
I think this is a case in which using explicit phylogenetic comparative methods might be useful. If all species were included in the species tree (rather than collapsed by clade as discussed above), and intron lengths were mapped onto the terminal branches of that phylogeny, ancestral character reconstruction could be performed to gain more explicit intuition as to whether independent expansions or contractions occurred, and how many times.
This could feasibly be done both using continuous measures of intron length, or alternatively by binning introns into "small" and "large" size categories (if intron length follows a bi-modal distribution for example), and using a discrete model of …
The driving mechanism for this trend may reflect one of two evolutionary scenarios: (a) intron expansion in Ev, or (b) intron contraction in S1/S2.
I think this is a case in which using explicit phylogenetic comparative methods might be useful. If all species were included in the species tree (rather than collapsed by clade as discussed above), and intron lengths were mapped onto the terminal branches of that phylogeny, ancestral character reconstruction could be performed to gain more explicit intuition as to whether independent expansions or contractions occurred, and how many times.
This could feasibly be done both using continuous measures of intron length, or alternatively by binning introns into "small" and "large" size categories (if intron length follows a bi-modal distribution for example), and using a discrete model of character transition to explicitly obtain counts of the number of transitions.
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For the S1, S2, Ev, and Po groups of Suessiales, the mean of isolate-specific protein families, and the mean ± standard deviation of estimated genome sizes are displayed.
Is there a reason why S1/S2 were collapsed, rather than showing all sampled Suessiales species the species tree? It seems this is a loss of information that would be nice to see in this early figure.
In particular, since Symbiodinium is not exclusively symbiotic, it would be informative to see how this life history is distributed within the group phylogenetically. Different phylogenetic histories and distributions of symbiosis could lead to alternative interpretations regarding the evolution of the life history, and consequently of the evolution of parasitism-associated genome size reduction.
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