Skip to main content Accessibility help
×
Home

Article contents

A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria

Published online by Cambridge University Press:  10 October 2018


D. S. Zarlenga
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
M. Mitreva
Affiliation:
The Genome Institute, Washington University School of Medicine, St. Louis, MO 63108, USA
P. Thompson
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
R. Tyagi
Affiliation:
The Genome Institute, Washington University School of Medicine, St. Louis, MO 63108, USA
W. Tuo
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
E. P. Hoberg
Affiliation:
USDA, Agricultural Research Service, Animal Parasitic Diseases Lab, Beltsville, MD 20705USA
Corresponding

Abstract

Horizontal gene transfer (HGT) has played an important role in the evolution of nematodes. Among candidate genes, cyanase, which is typically found only in plants, bacteria and fungi, is present in more than 35 members of the Phylum Nematoda, but absent from free-living and clade V organisms. Phylogenetic analyses showed that the cyanases of clade I organisms Trichinella spp., Trichuris spp. and Soboliphyme baturini (Subclass: Dorylaimia) represent a well-supported monophyletic clade with plant cyanases. In contrast, all cyanases found within the Subclass Chromadoria which encompasses filarioids, ascaridoids and strongyloids are homologous to those of bacteria. Western blots exhibited typical multimeric forms of the native molecule in protein extracts of Trichinella spiralis muscle larvae, where immunohistochemical staining localized the protein to the worm hypodermis and underlying muscle. Recombinant Trichinella cyanase was bioactive where gene transcription profiles support functional activity in vivo. Results suggest that: (1) independent HGT in parasitic nematodes originated from different Kingdoms; (2) cyanase acquired an active role in the biology of extant Trichinella; (3) acquisition occurred more than 400 million years ago (MYA), prior to the divergence of the Trichinellida and Dioctophymatida, and (4) early, free-living ancestors of the genus Trichinella had an association with terrestrial plants.


Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below.

References

Andersson, JO (2005) Lateral gene transfer in eukaryotes. Cellular and Molecular Life Sciences 62, 11821197.CrossRefGoogle ScholarPubMed
Anderson, PM and Little, RM (1986) Kinetic properties of cyanase. Biochemistry 25, 16211626.CrossRefGoogle ScholarPubMed
Anderson, IJ and Loftus, BJ (2005) Entamoeba histolytica: observations on metabolism based on the genome sequence. Experimental Parasitology 110, 173177.CrossRefGoogle ScholarPubMed
Anderson, PM, Sung, Y-C and Fuchs, JA (1990) The cyanase operon and cyanate metabolism. FEMS Microbiology Reviews 7, 247252.CrossRefGoogle ScholarPubMed
Blaxter, M (2007) Symbiont genes in host genomes: fragments with a future? Cell Host & Microbe 2, 211213.CrossRefGoogle ScholarPubMed
Blaxter, M (2011) Nematodes: the worm and its relatives. PLoS Biology 9, e1001050. https://doi.org/10.1371/journal.pbio.1001050.CrossRefGoogle ScholarPubMed
Blaxter, M, Koutsovoulos, G, Jones, M, Kumar, S and Elsworth, B (2014) Phylogenomics of Nematoda. In Cotton, J, Hughes, J and Olson, P (eds), Next-generation Systematics. Cambridge, UK: Cambridge University Press, pp. 6283. https://doi.org/10.1017/CBO9781139236355.004.Google Scholar
Bock, WJ (1959) Preadaptation and multiple evolutionary pathways. Evolution 13, 194211.CrossRefGoogle Scholar
Brooks, DR and McLennan, DA (2002) The Nature of Diversity: An Evolutionary Voyage of Discovery. Chicago, USA: University of Chicago Press.CrossRefGoogle Scholar
Crisp, A, Boschetti, C, Perry, M, Tunnacliffe, A and Micklem, G (2015) Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biology 16, 50.CrossRefGoogle Scholar
Dabert, M, Witalinski, W, Kazmierski, A, Olszanowski, Z and Dabert, J (2010) Molecular phylogeny of acariform mites (Acari, Arachnida): strong conflict between phylogenetic signal and long-branch attraction artifacts. Molecular Phylogenetics and Evolution 56, 222241.CrossRefGoogle ScholarPubMed
Dagan, T, Artzy-Randrup, Y and Martin, W (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proceedings of the National Academy of Sciences, USA 105, 1003910044.CrossRefGoogle ScholarPubMed
Dame, JB, Murrell, KD, Worley, DE and Schad, GA (1987) Trichinella spiralis: genetic evidence for synanthropic subspecies in sylvatic hosts. Experimental Parasitology 64, 195203.CrossRefGoogle ScholarPubMed
Danchin, EGJ, Perfus-Barbeoch, L, Rancurel, C, Thorpe, P, Da Rocha, M, Bajew, S, Neilson, R, Guzeeva, ES, Da Silva, C, Guy, J, Labadie, K, Esmenjaud, D, Helder, J, Jones, JT and den Akker, SE (2017) The transcriptomes of Xiphinema index and Longidorus elongatus suggest independent acquisition of some plant parasitism genes by horizontal gene transfer in early-branching nematodes. Genes (Basel) 8, E287.CrossRefGoogle ScholarPubMed
Dieterich, C and Sommer, RJ (2009) How to become a parasite – lessons from the genomes of nematodes. Trends in Genetics 25, 203209.CrossRefGoogle ScholarPubMed
Dieterich, C, Clifton, SW, Schuster, LN, Chinwalla, A, Delehaunty, K, Dinkelacker, I, Fulton, L, Fulton, R, Godfrey, J, Minx, P, Mitreva, M, Roeseler, W, Tian, H, Witte, H, Yang, SP, Wilson, RK and Sommer, RJ (2008) The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 11931198.CrossRefGoogle ScholarPubMed
Ebbs, S (2004) Biological degradation of cyanide compounds. Current Opinion in Biotechnology 15, 231236.CrossRefGoogle ScholarPubMed
el Kouni, MH (2017) Pyrimidine metabolism in schistosomes: a comparison with other parasites and the search for potential chemotherapeutic targets. Comparative Biochemistry and Physiology. Part B, Biochemistry & Molecular Biology 213, 5580.CrossRefGoogle ScholarPubMed
Elleuche, S and Pöggeler, S (2008) A cyanase is transcriptionally regulated by arginine and involved in cyanate decomposition in Sordaria macrospora. Fungal Genetics and Biology 45, 14581469.CrossRefGoogle ScholarPubMed
Elmore, MH, McGary, KL, Wisecaver, JH, Slot, JC, Geiser, DM, Sink, S, O'Donnell, K and Rokas, A (2015) Clustering of two genes putatively involved in cyanate detoxification evolved recently and independently in multiple fungal lineages. Genome Biology and Evolution 7, 789800.CrossRefGoogle ScholarPubMed
Espie, GS, Jalali, F, Tong, T, Zacal, NJ and So, AK (2007) Involvement of the cynABDS operon and the CO2-concentrating mechanism in the light-dependent transport and metabolism of cyanate by cyanobacteria. Journal of Bacteriology 189, 10131024.CrossRefGoogle ScholarPubMed
Gan, YH, Chua, KL, Chua, HH, Liu, B, Hii, CS, Chong, HL and Tan, P (2002) Characterization of Burkholderia pseudomallei infection and identification of novel virulence factors using a Caenorhabditis elegans host system. Molecular Microbiology 44, 11851197.CrossRefGoogle ScholarPubMed
Gilbert, A, Castro, J, Ferguson, JD and Gorden, C (1973) Amine excretion in excysted larvae and adults of Trichinella spiralis. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 45, 819828.Google Scholar
Guilloton, M and Karst, F (1987) Cyanate specifically inhibits arginine biosynthesis in Escherichia coli K12: a case of by-product inhibition? Journal of General Microbiology 133, 655665.Google ScholarPubMed
Guindon, S, Dufayard, JF, Lefort, V, Anisimova, M, Hordijk, W and Gascuel, O (2010) New algorithms and methods to estimate Maximum-Likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology 59, 307321.CrossRefGoogle ScholarPubMed
Haegeman, A, Jones, JT and Danchin, EGJ (2011) Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant-microbe Interactions 24, 879887.CrossRefGoogle ScholarPubMed
Haskins, WT and Weinstein, PP (1957) Nitrogenous excretory products of Trichinella spiralis larvae. Journal of Parasitology 43, 1924.CrossRefGoogle ScholarPubMed
Hewagama, A, Guy, HI, Vickrey, JF and Evans, DR (1999) Functional linkage between the glutaminase and synthetase domains of carbamoyl-phosphate synthetase. Role of serine 44 in carbamoyl-phosphate synthetase-aspartate carbamoyltransferase-dihydroorotase (cad). The Journal of Biological Chemistry 274, 2824028245.CrossRefGoogle Scholar
Holterman, M, van der Wurff, A, van den Elsen, S, van Megen, H, Bongers, T, Holovachov, O, Bakker, J and Helder, J (2006) Phylum-wide analysis of SSU rDNA reveals deep phylogenetic relationships among nematodes and accelerated evolution toward crown clades. Molecular Biology and Evolution 23, 17921800.CrossRefGoogle ScholarPubMed
Kamennaya, NA and Post, AF (2013) Distribution and expression of the cyanate acquisition potential among cyanobacterial populations in oligotrophic marine waters. Limnology and Oceanography 58, 19591971.CrossRefGoogle Scholar
Keeling, PJ and Palmer, JD (2008) Horizontal gene transfer in eukaryotic evolution. Nature Reviews. Genetics 9, 605618.CrossRefGoogle ScholarPubMed
Keen, NT and Roberts, PA (1998) Plant parasitic nematodes: digesting a page from the microbe book. Proceedings of the National Academy of Sciences, USA 95, 47894790.CrossRefGoogle ScholarPubMed
Kunz, DA and Nagappan, O (1989) Cyanase-mediated utilization of cyanate in Pseudomonas fluorescens. Applied and Environmental Microbiology 55, 256258.Google ScholarPubMed
Maeda, S and Omata, T (2009) Nitrite transport activity of the ABC-type cyanate transporter of the cyanobacterium Synechococcus elongatus. Journal of Bacteriology 191, 32653272.CrossRefGoogle ScholarPubMed
Marti, HP, Murrell, KD and Gamble, HR (1987) Trichinella spiralis: immunization of pigs with newborn larval antigens. Experimental Parasitology 63, 6873.CrossRefGoogle ScholarPubMed
McGill, LM, Fitzpatrick, DA, Pisani, D and Burnell, AM (2017) Estimation of phylogenetic divergence times in Panagrolaimidae and other nematodes using relaxed molecular clocks calibrated with insect and crustacean fossils. Nematology 19, 899913.CrossRefGoogle Scholar
Mitreva, M, Smant, G and Helder, J (2009) Role of horizontal gene transfer in the evolution of plant parasitism among nematodes. Methods in Molecular Biology 532, 517535.CrossRefGoogle ScholarPubMed
Mitreva, M, Jasmer, DP, Zarlenga, DS, Wang, Z, Abubucker, S, Martin, J, Taylor, CM, Yin, Y, Fulton, L, Minx, P, Yang, SP, Warren, WC, Fulton, RS, Bhonagiri, V, Zhang, X, Hallsworth-Pepin, K, Clifton, SW, McCarter, JP, Appleton, J, Mardis, ER and Wilson, RK (2011) The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228235.CrossRefGoogle ScholarPubMed
Mitreva-Dautova, M, Roze, E, Overmars, H, de Graaff, L, Schots, A, Helder, J, Goverse, A, Bakker, J and Smant, G (2006) A symbiont-independent endo-1,4-beta-xylanase from the plant-parasitic nematode Meloidogyne incognita. Molecular Plant-microbe Interactions 19, 521529.CrossRefGoogle ScholarPubMed
Morris, JL, Puttick, MN, Clark, JW, Edwards, D, Kenrick, P, Pressel, S, Wellman, CH, Yang, Z, Schneider, H and Donoghue, PCJ (2018) The timescale of early land plant evolution. Proceedings of the National Academy of Sciences, USA 115, E2274E2283.CrossRefGoogle ScholarPubMed
Nishikawa, BK, Fowlkes, DM and Kay, BK (1989) Convenient uses of polymerase chain reaction in analyzing recombinant cDNA clones. Biotechniques 7, 730735.Google ScholarPubMed
Opperman, CH, Bird, DM, Williamson, VM, Rokhsar, DS, Burke, M, Cohn, J, Cromer, J, Diener, S, Gajan, J, Graham, S, Houfek, TD, Liu, Q, Mitros, T, Schaff, J, Schaffer, R, Scholl, E, Sosinski, BR, Thomas, VP and Windham, E (2008) Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences, USA 105, 1480214807.CrossRefGoogle ScholarPubMed
Polz, MF, Alm, EJ and Hanage, WP (2013) Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends in Genetics 29, 170175.CrossRefGoogle ScholarPubMed
Rensing, SA, Lang, D, Zimmer, AD, Terry, A, Salamov, A, Shapiro, H, Nishiyama, T, Perroud, PF, Lindquist, EA, Kamisugi, Y, Tanahashi, T, Sakakibara, K, Fujita, T, Oishi, K, Shin-I, T, Kuroki, Y, Toyoda, A, Suzuki, Y, Hashimoto, S, Yamaguchi, K, Sugano, S, Kohara, Y, Fujiyama, A, Anterola, A, Aoki, S, Ashton, N, Barbazuk, WB, Barker, E, Bennetzen, JL, Blankenship, R, Cho, SH, Dutcher, SK, Estelle, M, Fawcett, JA, Gundlach, H, Hanada, K, Heyl, A, Hicks, KA, Hughes, J, Lohr, M, Mayer, K, Melkozernov, A, Murata, T, Nelson, DR, Pils, B, Prigge, M, Reiss, B, Renner, T, Rombauts, S, Rushton, PJ, Sanderfoot, A, Schween, G, Shiu, SH, Stueber, K, Theodoulou, FL, Tu, H, Van de Peer, Y, Verrier, PJ, Waters, E, Wood, A, Yang, L, Cove, D, Cuming, AC, Hasebe, M, Lucas, S, Mishler, BD, Reski, R, Grigoriev, IV, Quatrano, RS and Boore, JL (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science 319, 6469.CrossRefGoogle ScholarPubMed
Richards, TA, Dacks, JB, Jenkinson, JM, Thornton, CR and Talbot, NJ (2006) Evolution of filamentous plant pathogens: gene exchange across eukaryotic kingdoms. Current Biology 16, 18571864.CrossRefGoogle ScholarPubMed
Rödelsperger, C and Sommer, RJ (2011) Computational archaeology of the Pristionchus pacificus genome reveals evidence of horizontal gene transfers from insects. BioMed Central Evolutionary Biology 11, 239.Google ScholarPubMed
Sanderson, MJ, Thorne, JL, Wikstrom, N and Bremer, K (2004) Molecular evidence on plant divergence times. American Journal of Botany 91, 16561665.CrossRefGoogle ScholarPubMed
Schlachter, CR, Klapper, V, Wybouw, N, Radford, T, Van Leeuwen, T, Grbic, M and Chruszcz, M (2017) Structural characterization of a eukaryotic cyanase from Tetranychus urticae. Journal of Agricultural and Food Chemistry 65, 54535462.CrossRefGoogle ScholarPubMed
Smant, G, Stokkermans, JP, Yan, Y, de Boer, JM, Baum, TJ, Wang, X, Hussey, RS, Gommers, FJ, Henrissat, B, Davis, EL, Helder, J, Schots, A and Bakker, J (1998) Endogenous cellulases in animals: isolation of beta-1, 4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proceedings of the National Academy of Sciences, USA 9, 49064911.CrossRefGoogle Scholar
Walsh, MA, Otwinowski, Z, Perrakis, A, Anderson, PM and Joachimiak Andrzej, A (2000) Structure of cyanase reveals that a novel dimeric and decameric arrangement of subunits is required for formation of the enzyme active site. Structure 8, 505514.CrossRefGoogle ScholarPubMed
Wang, Z, Zarlenga, D, Martin, J, Abubucker, S and Mitreva, M (2012) Exploring metazoan evolution through dynamic and holistic changes in protein families and domains. BioMed Central Evolutionary Biology 12, 138.Google ScholarPubMed
Wybouw, N, Balabanidou, V, Ballhorn, DJ, Dermauw, W, Grbić, M, Vontas, J and Van Leeuwen, T (2012) A horizontally transferred cyanase gene in the spider mite Tetranychus urticae is involved in cyanate metabolism and is differentially expressed upon host plant change. Insect Biochemistry and Molecular Biology 42, 881889.CrossRefGoogle ScholarPubMed
Wybouw, N, Dermauw, W, Tirry, L, Stevens, C, Grbić, M, Feyereisen, R and Van Leeuwen, T (2014) A gene horizontally transferred from bacteria protects arthropods from host plant cyanide poisoning. eLIFE 3, e02365.CrossRefGoogle ScholarPubMed
Wybouw, N, Van Leeuwen, T and Dermauw, W (2018) A massive incorporation of microbial genes into the genome of Tetranychus urticae, a polyphagous arthropod herbivore. Insect Molecular Biology 27, 333351.CrossRefGoogle ScholarPubMed
Zarlenga, DS, Boyd, P, Lichtenfels, JR, Hill, D and Gamble, HR (2002) Identification and characterisation of a cDNA sequence encoding a glutamic acid-rich protein specifically transcribed in Trichinella spiralis newborn larvae and recognised by infected swine serum. International Journal for Parasitology 32, 13611370.CrossRefGoogle ScholarPubMed
Zarlenga, DS, Nisbet, AJ, Gasbarre, LC and Garrett, WM (2011) A calcium-activated nucleotidase secreted from Ostertagia ostertagi 4th-stage larvae is a member of the novel salivary apyrases present in blood-feeding arthropods. Parasitology 138, 333343.CrossRefGoogle ScholarPubMed
Zarlenga, D, Wang, Z and Mitreva, M (2016) Trichinella spiralis: adaptation and parasitism. Veterinary Parasitology 231, 821.CrossRefGoogle ScholarPubMed

Zarlenga et al. supplementary material

Zarlenga et al. supplementary material 1

[Opens in a new window]
File 781 KB

Altmetric attention score


Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 11
Total number of PDF views: 146 *
View data table for this chart

* Views captured on Cambridge Core between 10th October 2018 - 27th November 2020. This data will be updated every 24 hours.

Hostname: page-component-8465588854-jh7c5 Total loading time: 0.92 Render date: 2020-11-27T20:53:54.940Z Query parameters: { "hasAccess": "0", "openAccess": "0", "isLogged": "0", "lang": "en" } Feature Flags last update: Fri Nov 27 2020 20:12:13 GMT+0000 (Coordinated Universal Time) Feature Flags: { "metrics": true, "metricsAbstractViews": false, "peerReview": true, "crossMark": true, "comments": true, "relatedCommentaries": true, "subject": true, "clr": false, "languageSwitch": true }

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

A tale of three kingdoms: members of the Phylum Nematoda independently acquired the detoxifying enzyme cyanase through horizontal gene transfer from plants and bacteria
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *