skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Evolution of Protein-Mediated Biomineralization in Scleractinian Corals
While recent strides have been made in understanding the biological process by which stony corals calcify, much remains to be revealed, including the ubiquity across taxa of specific biomolecules involved. Several proteins associated with this process have been identified through proteomic profiling of the skeletal organic matrix (SOM) extracted from three scleractinian species. However, the evolutionary history of this putative “biomineralization toolkit,” including the appearance of these proteins’ throughout metazoan evolution, remains to be resolved. Here we used a phylogenetic approach to examine the evolution of the known scleractinians’ SOM proteins across the Metazoa. Our analysis reveals an evolutionary process dominated by the co-option of genes that originated before the cnidarian diversification. Each one of the three species appears to express a unique set of the more ancient genes, representing the independent co-option of SOM proteins, as well as a substantial proportion of proteins that evolved independently. In addition, in some instances, the different species expressed multiple orthologous proteins sharing the same evolutionary history. Furthermore, the non-random clustering of multiple SOM proteins within scleractinian-specific branches suggests the conservation of protein function between distinct species for what we posit is part of the scleractinian “core biomineralization toolkit.” This “core set” contains proteins that are likely fundamental to the scleractinian biomineralization mechanism. From this analysis, we infer that the scleractinians’ ability to calcify was achieved primarily through multiple lineage-specific protein expansions, which resulted in a new functional role that was not present in the parent gene.  more » « less
Award ID(s):
1939795
PAR ID:
10294881
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Frontiers in Genetics
Volume:
12
ISSN:
1664-8021
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Multicellular evolution is a major transition associated with momentous diversification of multiple lineages and increased developmental complexity. The volvocine algae comprise a valuable system for the study of this transition, as they span from unicellular to undifferentiated and differentiated multicellular morphologies despite their genomes being similar, suggesting multicellular evolution requires few genetic changes to undergo dramatic shifts in developmental complexity. Here, the evolutionary dynamics of six volvocine genomes were examined, where a gradual loss of genes was observed in parallel to the co-option of a few key genes. Protein complexes in the six species exhibited novel interactions, suggesting that gene loss could play a role in evolutionary novelty. This finding was supported by gene network modeling, where gene loss outpaces gene gain in generating novel stable network states. These results suggest gene loss, in addition to gene gain and co-option, may be important for the evolution developmental complexity. 
    more » « less
  2. Webster, Matthew (Ed.)
    Abstract The evolution of eusociality requires that individuals forgo some or all their own reproduction to assist the reproduction of others in their group, such as a primary egg-laying queen. A major open question is how genes and genetic pathways sculpt the evolution of eusociality, especially in rudimentary forms of sociality—those with smaller cooperative nests when compared with species such as honeybees that possess large societies. We lack comprehensive comparative studies examining shared patterns and processes across multiple social lineages. Here we examine the mechanisms of molecular convergence across two lineages of bees and wasps exhibiting such rudimentary societies. These societies consist of few individuals and their life histories range from facultative to obligately social. Using six species across four independent origins of sociality, we conduct a comparative meta-analysis of publicly available transcriptomes. Standard methods detected little similarity in patterns of differential gene expression in brain transcriptomes among reproductive and non-reproductive individuals across species. By contrast, both supervised machine learning and consensus co-expression network approaches uncovered sets of genes with conserved expression patterns among reproductive and non-reproductive phenotypes across species. These sets overlap substantially, and may comprise a shared genetic “toolkit” for sociality across the distantly related taxa of bees and wasps and independently evolved lineages of sociality. We also found many lineage-specific genes and co-expression modules associated with social phenotypes and possible signatures of shared life-history traits. These results reveal how taxon-specific molecular mechanisms complement a core toolkit of molecular processes in sculpting traits related to the evolution of eusociality. 
    more » « less
  3. Scleractinian corals typically form a robust calcium carbonate skeleton beneath their living tissue. This skeleton, through its trace element composition and isotope ratios, may record environmental conditions of water surrounding the coral animal. While bulk unrecrystallized aragonite coral skeletons can be used to reconstruct past ocean conditions, corals that have undergone significant diagenesis have altered geochemical signatures and are typically assumed to retain insufficient meaningful information for bulk or macrostructural analysis. However, partially recrystallized skeletons may retain organic molecular components of the skeletal organic matrix (SOM), which is secreted by the animal and directs aspects of the biomineralization process. Some SOM proteins can be retained in fossil corals and can potentially provide past oceanographic, ecological, and indirect genetic information. Here, we describe a dataset of scleractinian coral skeletons, aged from modern to Cretaceous plus a Carboniferous rugosan, characterized for their crystallography, trace element composition, and amino acid compositions. We show that some specimens that are partially recrystallized to calcite yield potentially useful biochemical information whereas complete recrystalization or silicification leads to significant alteration or loss of the SOM fraction. Our analysis is informative to biochemical-paleoceanographers as it suggests that previously discounted partially recrystallized coral skeletons may indeed still be useful at the microstructural level. 
    more » « less
  4. null (Ed.)
    One of the most fundamental and unresolved questions in evolutionary biology is whether the outcomes of evolution are predictable. Is the diversity of life we see today the expected result of organisms adapting to their environment throughout history (also known as natural selection) or the product of random chance? Or did chance events early in history shape the paths that evolution could take next, determining the biological forms that emerged under natural selection much later? These questions are hard to study because evolution happened only once, long ago. To overcome this barrier, Xie, Pu, Metzger et al. developed an experimental approach that can evolve reconstructed ancestral proteins that existed deep in the past. Using this method, it is possible to replay evolution multiple times, from various historical starting points, under conditions similar to those that existed long ago. The end products of the evolutionary trajectories can then be compared to determine how predictable evolution actually is. Xie, Pu, Metzger et al. studied proteins belonging to the BCL-2 family, which originated some 800 million years ago. These proteins have diversified greatly over time in both their genetic sequences and their ability to bind to specific partner proteins called co-regulators. Xie, Pu, Metzger et al. synthesized BCL-2 proteins that existed at various times in the past. Each ancestral protein was then allowed to evolve repeatedly under natural selection to acquire the same co-regulator binding functions that evolved during history. At the end of each evolutionary trajectory, the genetic sequence of the resulting BCL-2 proteins was recorded. This revealed that the outcomes of evolution were almost completely unpredictable: trajectories initiated from the same ancestral protein produced proteins with very different sequences, and proteins launched from different ancestral starting points were even more dissimilar. Further experiments identified the mutations in each trajectory that caused changes in coregulator binding. When these mutations were introduced into other ancestral proteins, they did not yield the same change in function. This suggests that early chance events influenced each protein’s evolution in an unpredictable way by opening and closing the paths available to it in the future. This research expands our understanding of evolution on a molecular level whilst providing a new experimental approach for studying evolutionary drivers in more detail. The results suggest that BCL-2 proteins, in all their various forms, are unique products of a particular, unpredictable course of history set in motion by ancient chance events. 
    more » « less
  5. Circulating hemocytes in the hemolymph represent the backbone of innate immunity in bivalves. Hemocytes are also found in the extrapallial fluid (EPF), the space delimited between the shell and the mantle, which is the site of shell biomineralization. This study investigated the transcriptome, proteome, and function of EPF and hemolymph in the hard clam Mercenaria mercenaria . Total and differential hemocyte counts were similar between EPF and hemolymph. Overexpressed genes in the EPF were found to have domains previously identified as being part of the “biomineralization toolkit” and involved in bivalve shell formation. Biomineralization related genes included chitin-metabolism genes, carbonic anhydrase, perlucin, and insoluble shell matrix protein genes. Overexpressed genes in the EPF encoded proteins present at higher abundances in the EPF proteome, specifically those related to shell formation such as carbonic anhydrase and insoluble shell matrix proteins. Genes coding for bicarbonate and ion transporters were also overexpressed, suggesting that EPF hemocytes are involved in regulating the availability of ions critical for biomineralization. Functional assays also showed that Ca 2+ content of hemocytes in the EPF were significantly higher than those in hemolymph, supporting the idea that hemocytes serve as a source of Ca 2+ during biomineralization. Overexpressed genes and proteins also contained domains such as C1q that have dual functions in biomineralization and immune response. The percent of phagocytic granulocytes was not significantly different between EPF and hemolymph. Together, these findings suggest that hemocytes in EPF play a central role in both biomineralization and immunity. 
    more » « less