Stress Adapted Mollusca and Nematoda Exhibit Convergently Expanded Hsp70 and AIG1 Gene Families

Guerin, Megan N.; Weinstein, Deborah J.; Bracht, John R.

doi:10.1007/s00239-019-09900-9

Cited by 19 publications

(19 citation statements)

References 60 publications

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“…They are lacking as far as is known in representative fungi like yeast like Saccharomyces cerevisae, early diverging metazoans such as the placozoan Trichoplax or the sponge Amphimedon, or in the model ecdysozoans Caenorhabditis elegans or Drosophila melanogaster. A recent study predicted 60 AIG1 genes in the genome of the subterrestrial, thermally-stressed nematode Halicephalobus mephisto [27]. In deuterostomes, they are not known from the tunicate Ciona, the sea urchin Strongylocentrotus or from lampreys [19,23].…”

Section: Introductionmentioning

confidence: 99%

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Genome-wide discovery, and computational and transcriptional characterization of an AIG gene family in the freshwater snail Biomphalaria glabrata, a vector for Schistosoma mansoni

Loker

Zhang

et al. 2020

BMC Genomics

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Background: The AIG (avrRpt2-induced gene) family of GTPases, characterized by the presence of a distinctive AIG1 domain, is mysterious in having a peculiar phylogenetic distribution, a predilection for undergoing expansion and loss, and an uncertain functional role, especially in invertebrates. AIGs are frequently represented as GIMAPs (GTPase of the immunity associated protein family), characterized by presence of the AIG1 domain along with coiled-coil domains. Here we provide an overview of the remarkably expanded AIG repertoire of the freshwater gastropod Biomphalaria glabrata, compare it with AIGs in other organisms, and detail patterns of expression in B. glabrata susceptible or resistant to infection with Schistosoma mansoni, responsible for the neglected tropical disease of intestinal schistosomiasis. Results: We define the 7 conserved motifs that comprise the AIG1 domain in B. glabrata and detail its association with at least 7 other domains, indicative of functional versatility of B. glabrata AIGs. AIG genes were usually found in tandem arrays in the B. glabrata genome, suggestive of an origin by segmental gene duplication. We found 91 genes with complete AIG1 domains, including 64 GIMAPs and 27 AIG genes without coiled-coils, more than known for any other organism except Danio (with > 100). We defined expression patterns of AIG genes in 12 different B. glabrata organs and characterized whole-body AIG responses to microbial PAMPs, and of schistosome-resistant or-susceptible strains of B. glabrata to S. mansoni exposure. Biomphalaria glabrata AIG genes clustered with expansions of AIG genes from other heterobranch gastropods yet showed unique lineage-specific subclusters. Other gastropods and bivalves had separate but also diverse expansions of AIG genes, whereas cephalopods seem to lack AIG genes. Conclusions: The AIG genes of B. glabrata exhibit expansion in both numbers and potential functions, differ markedly in expression between strains varying in susceptibility to schistosomes, and are responsive to immune challenge. These features provide strong impetus to further explore the functional role of AIG genes in the defense responses of B. glabrata, including to suppress or support the development of medically relevant S. mansoni parasites.

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Section: Introductionmentioning

confidence: 99%

“…Rats have 7 genes, humans 8 and mice 9 [29,30]. AIG gene family expansions have occurred in bivalves and in the nematode H. mephisto [19,23,27]. GIMAP loci are clustered in plants, corals and mammals, suggestive of tandem gene duplications [16,23,28,29].…”

Section: Introductionmentioning

confidence: 99%

Genome-wide discovery, and computational and transcriptional characterization of an AIG gene family in the freshwater snail Biomphalaria glabrata, a vector for Schistosoma mansoni

Loker

Zhang

et al. 2020

BMC Genomics

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“…We note that the pacific oyster Crassostrea gigas has convergently expanded Hsp70 and AIG1 gene families 83 and activates the UPR in response to abiotic stress including heat 84 , so H. mephisto helps define a general evolutionary adaptive response to heat stress 85 . While the oyster experiences considerable thermal fluctuation, H. mephisto does not, as described above.…”

Section: Discussionmentioning

confidence: 95%

The genome of a subterrestrial nematode reveals adaptations to heat

et al. 2019

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The nematode Halicephalobus mephisto was originally discovered inhabiting a deep terrestrial aquifer 1.3 km underground. H. mephisto can thrive under conditions of abiotic stress including heat and minimal oxygen, where it feeds on a community of both chemolithotrophic and heterotrophic prokaryotes in an unusual ecosystem isolated from the surface biosphere. Here we report the comprehensive genome and transcriptome of this organism, identifying a signature of adaptation: an expanded repertoire of 70 kilodalton heat-shock proteins (Hsp70) and avrRpt2 induced gene 1 (AIG1) proteins. The expanded Hsp70 genes are transcriptionally induced upon growth under heat stress, and we find that positive selection is detectable in several members of this family. We further show that AIG1 may have been acquired by horizontal gene transfer (HGT) from a rhizobial fungus. Over one-third of the genes of H. mephisto are novel, highlighting the divergence of this nematode from other sequenced organisms. This work sheds light on the genomic basis of heat tolerance in a complete subterrestrial eukaryotic genome.

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“…As an assay for the impact of hemizygosity on gene duplication rates and gene evolution more generally, we have studied in detail two gene families where multiple genes were found in hemizygous regions in multiple species, the HSP70 superfamily and the C1qDC containing genes. These are involved in resilience to stress and are important pattern recognition receptors in innate immunity of invertebrates, respectively [54][55][56][57], and it is possible that PAV in hemizygous regions is linked to differential adaptive capacity across the ranges of these genes.…”

Section: Individual Gene Families Hemizygosity and Pavmentioning

confidence: 99%

Single individual structural variant detection uncovers widespread hemizygosity in molluscs

Calcino

Kenny

Gerdol

2021

Phil. Trans. R. Soc. B

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The advent of complete genomic sequencing has opened a window into genomic phenomena obscured by fragmented assemblies. A good example of these is the existence of hemizygous regions of autosomal chromosomes, which can result in marked differences in gene content between individuals within species. While these hemizygous regions, and presence/absence variation of genes that can result, are well known in plants, firm evidence has only recently emerged for their existence in metazoans. Here, we use recently published, complete genomes from wild-caught molluscs to investigate the prevalence of hemizygosity across a well-known and ecologically important clade. We show that hemizygous regions are widespread in mollusc genomes, not clustered in individual chromosomes, and often contain genes linked to transposition, DNA repair and stress response. With targeted investigations of HSP70-12 and C1qDC , we also show how individual gene families are distributed within pan-genomes. This work suggests that extensive pan-genomes are widespread across the conchiferan Mollusca, and represent useful tools for genomic evolution, allowing the maintenance of additional genetic diversity within the population. As genomic sequencing and re-sequencing becomes more routine, the prevalence of hemizygosity, and its impact on selection and adaptation, are key targets for research across the tree of life. This article is part of the Theo Murphy meeting issue ‘Molluscan genomics: broad insights and future directions for a neglected phylum’.

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Stress Adapted Mollusca and Nematoda Exhibit Convergently Expanded Hsp70 and AIG1 Gene Families

Cited by 19 publications

References 60 publications

Genome-wide discovery, and computational and transcriptional characterization of an AIG gene family in the freshwater snail Biomphalaria glabrata, a vector for Schistosoma mansoni

Genome-wide discovery, and computational and transcriptional characterization of an AIG gene family in the freshwater snail Biomphalaria glabrata, a vector for Schistosoma mansoni

The genome of a subterrestrial nematode reveals adaptations to heat

Single individual structural variant detection uncovers widespread hemizygosity in molluscs

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