An official website of the United States government
Abstract Background Calcareous outcrops, rocky areas composed of calcium carbonate (CaCO 3 ), often host a diverse, specialized, and threatened biomineralizing fauna. Despite the repeated evolution of physiological and morphological adaptations to colonize these mineral rich substrates, there is a lack of genomic resources for calcareous rock endemic species. This has hampered our ability to understand the genomic mechanisms underlying calcareous rock specialization and manage these threatened species. Results Here, we present a new draft genome assembly of the threatened limestone endemic land snail Oreohelix idahoensis and genome skim data for two other Oreohelix species. The O. idahoensis genome assembly (scaffold N50: 404.19 kb; 86.6% BUSCO genes) is the largest (~ 5.4 Gb) and most repetitive mollusc genome assembled to date (85.74% assembly size). The repetitive landscape was unusually dominated by an expansion of long terminal repeat (LTR) transposable elements (57.73% assembly size) which have shaped the evolution genome size, gene composition through retrotransposition of host genes, and ectopic recombination. Genome skims revealed repeat content is more than 2–3 fold higher in limestone endemic O. idahoensis compared to non-calcareous Oreohelix species. Gene family size analysis revealed stress and biomineralization genes have expanded significantly in the O. idahoensis genome . Conclusions Hundreds of threatened land snail species are endemic to calcareous rock regions but there are very few genomic resources available to guide their conservation or determine the genomic architecture underlying CaCO 3 resource specialization. Our study provides one of the first high quality draft genomes of a calcareous rock endemic land snail which will serve as a foundation for the conservation genomics of this threatened species and for other groups. The high proportion and activity of LTRs in the O. idahoensis genome is unprecedented in molluscan genomics and sheds new light how transposable element content can vary across molluscs. The genomic resources reported here will enable further studies of the genomic mechanisms underlying calcareous rock specialization and the evolution of transposable element content across molluscs.
more »
« less
The Iron-Responsive Genome of the Chiton Acanthopleura granulata
Abstract Molluscs biomineralize structures that vary in composition, form, and function, prompting questions about the genetic mechanisms responsible for their production and the evolution of these mechanisms. Chitons (Mollusca, Polyplacophora) are a promising system for studies of biomineralization because they build a range of calcified structures including shell plates and spine- or scale-like sclerites. Chitons also harden the calcified teeth of their rasp-like radula with a coat of iron (as magnetite). Here we present the genome of the West Indian fuzzy chiton Acanthopleura granulata, the first from any aculiferan mollusc. The A. granulata genome contains homologs of many genes associated with biomineralization in conchiferan molluscs. We expected chitons to lack genes previously identified from pathways conchiferans use to make biominerals like calcite and nacre because chitons do not use these materials in their shells. Surprisingly, the A. granulata genome has homologs of many of these genes, suggesting that the ancestral mollusc may have had a more diverse biomineralization toolkit than expected. The A. granulata genome has features that may be specialized for iron biomineralization, including a higher proportion of genes regulated directly by iron than other molluscs. A. granulata also produces two isoforms of soma-like ferritin: one is regulated by iron and similar in sequence to the soma-like ferritins of other molluscs, and the other is constitutively translated and is not found in other molluscs. The A. granulata genome is a resource for future studies of molluscan evolution and biomineralization.
more »
« less
- Award ID(s):
- 1846174
- PAR ID:
- 10290880
- Editor(s):
- Venkatesh, B
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Synopsis The gastropod shell is a composite composed of minerals and shell matrix proteins (SMPs). SMPs have been identified by proteomics in many molluscs, but few have been studied in detail. Open questions include (1) what gene regulatory networks regulate SMP expression, (2) what roles individual SMPs play in biomineralization, and (3) how the complement of SMPs changes over development. These questions are best addressed in a species in which gene perturbation studies are available; one such species is the slipper snail, Crepidula fornicata. Here, SEM and pXRD analysis demonstrated that the adult shell of C. fornicata exhibits crossed lamellar microstructure and is composed of aragonite. Using high-throughput proteomics we identified 185 SMPs occluded within the adult shell. Over half of the proteins in the shell proteome have known biomineralization domains, while at least 10% have no homologs in public databases. Differential gene expression analysis identified 20 SMP genes that are up-regulated in the shell-producing mantle tissue. Over half of these 20 SMPs are expressed during development with two, CfSMP1 and CfSMP2, expressed exclusively in the shell gland. Together, the description of the shell microstructure and a list of SMPs now sets the stage for studying the consequences of SMP gene knockdowns in molluscs.more » « less
-
Gene amplification has been observed in many bacteria and eukaryotes as a response to various selective pressures, such as antibiotics, cytotoxic drugs, pesticides, herbicides, and other stressful environmental conditions. An increase in gene copy number is often found as extrachromosomal elements that usually contain autonomously replicating extrachromosomal circular DNA molecules (eccDNAs). Amaranthus palmeri , a crop weed, can develop herbicide resistance to glyphosate [ N -(phosphonomethyl) glycine] by amplification of the 5-enolpyruvylshikimate-3-phosphate synthase ( EPSPS ) gene, the molecular target of glyphosate. However, biological questions regarding the source of the amplified EPSPS , the nature of the amplified DNA structures, and mechanisms responsible for maintaining this gene amplification in cells and their inheritance remain unknown. Here, we report that amplified EPSPS copies in glyphosate-resistant (GR) A. palmeri are present in the form of eccDNAs with various conformations. The eccDNAs are transmitted during cell division in mitosis and meiosis to the soma and germ cells and the progeny by an as yet unknown mechanism of tethering to mitotic and meiotic chromosomes. We propose that eccDNAs are one of the components of McClintock’s postulated innate systems [McClintock B (1978) Stadler Genetics Symposium ] that can rapidly produce soma variation, amplify EPSPS genes in the sporophyte that are transmitted to germ cells, and modulate rapid glyphosate resistance through genome plasticity and adaptive evolution.more » « less
-
Mollusca is the second most species-rich phylum and includes animals as disparate as octopuses, clams, and chitons. Dozens of molluscan genomes are available, but only one representative of the subphylum Aculifera, the sister taxon to all other molluscs, has been sequenced to date, hindering comparative and evolutionary studies. To facilitate evolutionary studies across Mollusca, we sequenced the genome of a second aculiferan mollusc, the lepidopleurid chiton Hanleya hanleyi (Bean 1844), using a hybrid approach combining Oxford Nanopore and Illumina reads. After purging redundant haplotigs and removing contamination from this 1.3% heterozygous genome, we produced a 2.5 Gbp haploid assembly (>4X the size of the other chiton genome sequenced to date) with an N50 of 65.0 Kbp. Despite a fragmented assembly, the genome is rather complete (92.0% of BUSCOs detected; 79.4% complete plus 12.6% fragmented). Remarkably, the genome has the highest repeat content of any molluscan genome reported to date (>66%). Our gene annotation pipeline predicted 69,284 gene models (92.9% of BUSCOs detected; 81.8% complete plus 11.1% fragmented) of which 35,362 were supported by transcriptome and/or protein evidence. Phylogenomic analysis recovered Polyplacophora sister to all other sampled molluscs with maximal support. The Hanleya genome will be a valuable resource for studies of molluscan biology with diverse potential applications ranging from evolutionary and comparative genomics to molecular ecology.more » « less
-
Mitchell, Aaron P. (Ed.)ABSTRACT TUP1 is a well-characterized repressor of transcription in Saccharomyces cerevisiae and Candida albicans and is observed as a single-copy gene. We observe that most species that experienced a whole-genome duplication outside of the Saccharomyces genus have two copies of TUP1 in the Saccharomycotina yeast clade. We focused on Candida glabrata and demonstrated that the uncharacterized TUP1 homolog, C. glabrata TUP11 ( CgTUP11 ), is most like the S. cerevisiae TUP1 ( ScTUP1 ) gene through phenotypic assays and transcriptome sequencing (RNA-seq). Whereas CgTUP1 plays a role in gene repression, it is much less repressive in standard growth media. Through RNA-seq and reverse transcription-quantitative PCR (RT-qPCR), we observed that genes associated with pathogenicity ( YPS2 , YPS4 , and HBN1 ) are upregulated upon deletion of either paralog, and loss of both paralogs is synergistic. Loss of the corepressor CgCYC8 mimics the loss of both paralogs, but not to the same extent as the Cgtup1 Δ Cgtup11 Δ mutant for these pathogenesis-related genes. In contrast, genes involved in energy metabolism ( CgHXT2 , CgADY2 , and CgFBP1 ) exhibit similar behavior (dependence on both paralogs), but deletion of CgCYC8 is very similar to the Cgtup1 Δ Cgtup11 Δ mutant. Finally, some genes ( CgMFG1 and CgRIE1 ) appear to only be dependent on CgTUP11 and CgCYC8 and not CgTUP1 . These data indicate separable and overlapping roles for the two TUP1 paralogs and that other genes may function as the Cg Cyc8 corepressor. Through a comparison by RNA-seq of Sctup1 Δ, it was found that TUP1 homologs regulate similar genes in the two species. This work highlights that studies focused only on Saccharomyces may miss important biological processes because of paralog loss after genome duplication. IMPORTANCE Due to a whole-genome duplication, many yeast species related to C. glabrata have two copies of the well-characterized TUP1 gene, unlike most Saccharomyces species. This work identifies roles for the paralogs in C. glabrata , highlights the importance of the uncharacterized paralog, called TUP11 , and suggests that the two paralogs have both overlapping and unique functions. The TUP1 paralogs likely influence pathogenicity based on tup mutants upregulating genes that are associated with pathogenicity.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/gbe/evaa263
