Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Pavla Bartošová-Sojková; Jiří Kyslík; Gema Alama-Bermejo; Ashlie Hartigan; Stephen D Atkinson; Jerri L Bartholomew; Amparo Picard-Sánchez; Oswaldo Palenzuela; Marc Nicolas Faber; Jason W Holland; Astrid S Holzer

doi:10.3390/biology10020110

Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Pavla Bartošová-Sojková^* (Corresponding Author), Jiří Kyslík, Gema Alama-Bermejo, Ashlie Hartigan, Stephen D Atkinson, Jerri L Bartholomew, Amparo Picard-Sánchez, Oswaldo Palenzuela, Marc Nicolas Faber, Jason W Holland, Astrid S Holzer

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.

Original language	English
Article number	110
Number of pages	16
Journal	Biology
Volume	10
Issue number	2
DOIs	https://doi.org/10.3390/biology10020110
Publication status	Published - 3 Feb 2021

Bibliographical note

Acknowledgments: We thank to Baveesh Pudhuvai (BC CAS, Budweis, Czech Republic) for help in the PCR verification of Buddenbrockia stefin. We also thank Ivan Fiala (BC CAS, Budweis, Czech Republic) for providing suggestions to improve the manuscript and for sharing M. lieberkuehni and N. pickii transcriptomic data. We are grateful to Hanna Hartikainen (ETH Zurich, Switzerland) for sharing T. bryosalmonae genome data.

Funding: This research was funded by the Ministry of Education, Youth, and Sports of the Czech Republic, grant number LTAUSA17201; by the European Commission under the H2020 Programme— ParaFishControl, grant number 634429; by the Czech Science Foundation, grant number 19-28399X (to A. S. Holzer, G. Alama-Bermejo, and J. Kyslík) and 21-16565S and by the Czech Academy of Sciences and Hungarian Academy of Sciences, grant number MTA 19-07. This publication reflects the views of the authors only; the European Commission cannot be held responsible for any use which may be made of the information contained therein.

Keywords

Cysteine protease inhibitor
Diversification
Parasite
Phylogenetic analysis
Protein structure
Signal peptide
Stefin

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Bartošová-Sojková, P., Kyslík, J., Alama-Bermejo, G., Hartigan, A., Atkinson, S. D., Bartholomew, J. L., Picard-Sánchez, A., Palenzuela, O., Faber, M. N., Holland, J. W., & Holzer, A. S. (2021). Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians. Biology, 10(2), Article 110. https://doi.org/10.3390/biology10020110

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title = "Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians",

abstract = "The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.",

keywords = "Cysteine protease inhibitor, Diversification, Parasite, Phylogenetic analysis, Protein structure, Signal peptide, Stefin",

author = "Pavla Barto{\v s}ov{\'a}-Sojkov{\'a} and Ji{\v r}{\'i} Kysl{\'i}k and Gema Alama-Bermejo and Ashlie Hartigan and Atkinson, {Stephen D} and Bartholomew, {Jerri L} and Amparo Picard-S{\'a}nchez and Oswaldo Palenzuela and Faber, {Marc Nicolas} and Holland, {Jason W} and Holzer, {Astrid S}",

note = "Acknowledgments: We thank to Baveesh Pudhuvai (BC CAS, Budweis, Czech Republic) for help in the PCR verification of Buddenbrockia stefin. We also thank Ivan Fiala (BC CAS, Budweis, Czech Republic) for providing suggestions to improve the manuscript and for sharing M. lieberkuehni and N. pickii transcriptomic data. We are grateful to Hanna Hartikainen (ETH Zurich, Switzerland) for sharing T. bryosalmonae genome data. Funding: This research was funded by the Ministry of Education, Youth, and Sports of the Czech Republic, grant number LTAUSA17201; by the European Commission under the H2020 Programme— ParaFishControl, grant number 634429; by the Czech Science Foundation, grant number 19-28399X (to A. S. Holzer, G. Alama-Bermejo, and J. Kysl{\'i}k) and 21-16565S and by the Czech Academy of Sciences and Hungarian Academy of Sciences, grant number MTA 19-07. This publication reflects the views of the authors only; the European Commission cannot be held responsible for any use which may be made of the information contained therein.",

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doi = "10.3390/biology10020110",

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T1 - Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

AU - Bartošová-Sojková, Pavla

AU - Kyslík, Jiří

AU - Alama-Bermejo, Gema

AU - Hartigan, Ashlie

AU - Atkinson, Stephen D

AU - Bartholomew, Jerri L

AU - Picard-Sánchez, Amparo

AU - Palenzuela, Oswaldo

AU - Faber, Marc Nicolas

AU - Holland, Jason W

AU - Holzer, Astrid S

N1 - Acknowledgments: We thank to Baveesh Pudhuvai (BC CAS, Budweis, Czech Republic) for help in the PCR verification of Buddenbrockia stefin. We also thank Ivan Fiala (BC CAS, Budweis, Czech Republic) for providing suggestions to improve the manuscript and for sharing M. lieberkuehni and N. pickii transcriptomic data. We are grateful to Hanna Hartikainen (ETH Zurich, Switzerland) for sharing T. bryosalmonae genome data. Funding: This research was funded by the Ministry of Education, Youth, and Sports of the Czech Republic, grant number LTAUSA17201; by the European Commission under the H2020 Programme— ParaFishControl, grant number 634429; by the Czech Science Foundation, grant number 19-28399X (to A. S. Holzer, G. Alama-Bermejo, and J. Kyslík) and 21-16565S and by the Czech Academy of Sciences and Hungarian Academy of Sciences, grant number MTA 19-07. This publication reflects the views of the authors only; the European Commission cannot be held responsible for any use which may be made of the information contained therein.

PY - 2021/2/3

Y1 - 2021/2/3

N2 - The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.

AB - The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.

KW - Cysteine protease inhibitor

KW - Diversification

KW - Parasite

KW - Phylogenetic analysis

KW - Protein structure

KW - Signal peptide

KW - Stefin

U2 - 10.3390/biology10020110

DO - 10.3390/biology10020110

M3 - Article

C2 - 33546310

SN - 2079-7737

VL - 10

JO - Biology

JF - Biology

IS - 2

M1 - 110

ER -

Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Abstract

Bibliographical note

Keywords

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