Skip to main content
×
×
Home

Host–symbiont–pathogen interactions in blood-feeding parasites: nutrition, immune cross-talk and gene exchange

  • Filip Husnik (a1)
Abstract

Animals are common hosts of mutualistic, commensal and pathogenic microorganisms. Blood-feeding parasites feed on a diet that is nutritionally unbalanced and thus often rely on symbionts to supplement essential nutrients. However, they are also of medical importance as they can be infected by pathogens such as bacteria, protists or viruses that take advantage of the blood-feeding nutritional strategy for own transmission. Since blood-feeding evolved multiple times independently in diverse animals, it showcases a gradient of host–microbe interactions. While some parasitic lineages are possibly asymbiotic and manage to supplement their diet from other food sources, other lineages are either loosely associated with extracellular gut symbionts or harbour intracellular obligate symbionts that are essential for the host development and reproduction. What is perhaps even more diverse are the pathogenic lineages that infect blood-feeding parasites. This microbial diversity not only puts the host into a complicated situation – distinguishing between microorganisms that can greatly decrease or increase its fitness – but also increases opportunity for horizontal gene transfer to occur in this environment. In this review, I first introduce this diversity of mutualistic and pathogenic microorganisms associated with blood-feeding animals and then focus on patterns in their interactions, particularly nutrition, immune cross-talk and gene exchange.

Copyright
Corresponding author
Author for correspondence: Filip Husnik, E-mail: filip.husnik@gmail.com
References
Hide All
Adams, TS (1999) Hematophagy and hormone release. Annals of the Entomological Society of America 92, 113.
Akman, L, et al. (2002) Genome sequence of the endocellular obligate symbiont of tsetse flies, Wigglesworthia glossinidia. Nature Genetics 32, 402407.
Alexander, WG, et al. (2016) Horizontally acquired genes in early-diverging pathogenic fungi enable the use of host nucleosides and nucleotides. Proceedings of the National Academy of Sciences 113, 41164121.
Aschner, M (1932) Experimentelle unter suchungen über die symbiose der kleiderlaus. Naturwissenschaften 20, 501505.
Balmand, S, et al. (2013) Tissue distribution and transmission routes for the tsetse fly endosymbionts. Journal of Invertebrate Pathology 112, S116S122.
Bänziger, H (1975) Skin-piercing blood-sucking moths I: ecological and ethological studies on Calpe eustrigata (Lepid., Noctuidae). Acta Tropica 32, 125144.
Beard, CB, Cordon-Rosales, C and Durvasula, RV (2002) Bacterial symbionts of the riatominae and their potential use in control of Chagas disease transmission. Annual Review of Entomology 47, 123141.
Becnel, JJ, White, SE and Shapiro, AM (2005) Review of microsporidia-mosquito relationships: from the simple to the complex. Folia Parasitologica 52, 4150.
Benoit, JB, et al. (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nature Communications 7, 10165.
Berasategui, A, et al. (2015) Potential applications of insect symbionts in biotechnology. Applied Microbiology and Biotechnology 100, 15671577.
Bing, X, et al. (2017) Unravelling the relationship between the tsetse fly and its obligate symbiont Wigglesworthia: transcriptomic and metabolomic landscapes reveal highly integrated physiological networks. Proceedings of the Royal Society B-Biological Sciences 284, pii: 20170360.
Bordenstein, SR and Wernegreen, JJ (2004) Bacteriophage flux in endosymbionts (Wolbachia): infection frequency, lateral transfer, and recombination rates. Molecular Biology and Evolution 21, 19811991.
Boyd, BM, et al. (2014) Genome sequence of Candidatus Riesia pediculischaeffi, endosymbiont of chimpanzee lice, and genomic comparison of recently acquired endosymbionts from human and chimpanzee lice. G3 4, 21892195.
Boyd, BM, et al. (2016) Two bacterial genera, Sodalis and Rickettsia, associated with the seal louse Proechinophthirus fluctus (Phthiraptera: Anoplura). Applied and Environmental Microbiology 82, 31853197.
Boyd, BM, et al. (2017) Primates, lice and bacteria: speciation and genome evolution in the symbionts of hominid lice. Molecular Biology and Evolution 34, 17431757.
Brecher, G and Wigglesworth, VB (1944) The transmission of Actinomyces rhodnii Erikson in Rhodnius prolixus Stål (Hemiptera) and its influence on the growth of the host. Parasitology 35, 220224.
Brelsfoard, C, et al. (2014) Presence of extensive Wolbachia symbiont insertions discovered in the genome of its host Glossina morsitans morsitans. PLoS Neglected Tropical Diseases 8, e2728.
Buchner, P (1965) Endosymbiosis of Animals with Plant Microorganisms. New York: Interscience Publishers.
Capone, A, et al. (2013) Interactions between Asaia, Plasmodium and Anopheles: new insights into mosquito symbiosis and implications in malaria symbiotic control. Parasites & Vectors 6, 182.
Carrillo-Araujo, M, et al. (2015) Phyllostomid bat microbiome composition is associated to host phylogeny and feeding strategies. Frontiers in Microbiology 6, 447.
Chou, S, et al. (2014) Transferred interbacterial antagonism genes augment eukaryotic innate immune function. Nature 518, 98101.
Coon, KL, et al. (2014) Mosquitoes rely on their gut microbiota for development. Molecular Ecology 23, 27272739.
Coon, KL, et al. (2017) Bacteria-mediated hypoxia functions as a signal for mosquito development. Proceedings of the National Academy of Sciences of the USA 14(27), E5362E5369.
da Mota, FF, et al. (2012) Cultivation-independent methods reveal differences among bacterial gut microbiota in triatomine vectors of Chagas disease. PLoS Neglected Tropical Diseases 6, e1631.
Damiani, C, et al. (2010) Mosquito-bacteria symbiosis: the case of Anopheles gambiae and Asaia. Microbial Ecology 60, 644654.
De Vooght, L, et al. (2014) Delivery of a functional anti-trypanosome nanobody in different tsetse fly tissues via a bacterial symbiont, Sodalis glossinidius. Microbial Cell Factories 13, 156.
Dheilly, NM, et al. (2017) Parasite microbiome project: systematic investigation of microbiome dynamics within and across parasite-host interactions. mSystems 2, e0005017.
Douglas, AE (2017) The B vitamin nutrition of insects: the contributions of diet, microbiome and horizontally acquired genes. Current Opinion in Insect Science 23, 6569.
Duron, O, et al. (2017) Evolutionary changes in symbiont community structure in ticks. Molecular Ecology 26, 29052921.
Eggers, CH, et al. (2016) Phage-mediated horizontal gene transfer of both prophage and heterologous DNA by ϕBB-1, a bacteriophage of Borrelia burgdorferi. Pathogens and Disease 74, ftw107.
Eichler, S and Schaub, GA (2002) Development of symbionts in triatomine bugs and the effects of infections with trypanosomatids. Experimental Parasitology 100, 1727.
Eme, L, et al. (2017) Lateral gene transfer in the adaptation of the anaerobic parasite Blastocystis to the gut. Current Biology 27, 807820.
Engel, P and Moran, NA (2013) The gut microbiota of insects – diversity in structure and function. FEMS Microbiology Reviews 37, 699735.
Enomoto, S, et al. (2017) Quorum sensing attenuates virulence in Sodalis praecaptivus. Cell Host & Microbe 21, 629636.
Fontaine, A, et al. (2011) Implication of haematophagous arthropod salivary proteins in host-vector interactions. Parasites & Vectors 4, 187.
Geiger, A, et al. (2016) Escaping deleterious immune response in their hosts: lessons from trypanosomatids. Frontiers in Immunology 7, 212.
Gerardo, NM, et al. (2010) Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biology 11, R21.
Gerhart, JG, Moses, AS and Raghavan, R (2016) A Francisella-like endosymbiont in the Gulf Coast tick evolved from a mammalian pathogen. Scientific Reports 6, 33670.
Gerth, M and Bleidorn, C (2016) Comparative genomics provides a timeframe for Wolbachia evolution and exposes a recent biotin synthesis operon transfer. Nature Microbiology 2, 16241.
Gillespie, JJ, et al. (2012) A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. Journal of Bacteriology 194, 376394.
Gottlieb, Y, Lalzar, I and Klasson, L (2015) Distinctive genome reduction rates revealed by genomic analyses of two Coxiella-like endosymbionts in ticks. Genome Biology and Evolution 7, 17791796.
Graça-Souza, AV, et al. (2006) Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochemistry and Molecular Biology 36, 322335.
Guy, L, et al. (2013) A gene transfer agent and a dynamic repertoire of secretion systems hold the keys to the explosive radiation of the emerging pathogen Bartonella. PLoS Genetics 9, e1003393.
Hansen, AK and Moran, NA (2011) Aphid genome expression reveals host-symbiont cooperation in the production of amino acids. Proceedings of the National Academy of Sciences of the USA 108, 28492854.
Hoffmann, AA, et al. (2011) Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476, 454457.
Hosokawa, T, et al. (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proceedings of the National Academy of Sciences of the USA 107, 769774.
Hosokawa, T, et al. (2012) Reductive genome evolution, host-symbiont co-speciation and uterine transmission of endosymbiotic bacteria in bat flies. The ISME Journal 6, 577587.
Huang, J (2013) Horizontal gene transfer in eukaryotes: the weak-link model. BioEssays 35, 868875.
Husnik, F and McCutcheon, JP (2016) Repeated replacement of an intrabacterial symbiont in the tripartite nested mealybug symbiosis. Proceedings of the National Academy of Sciences of the USA 113, E5416E5424.
Husnik, F and McCutcheon, JP (2018) Functional horizontal gene transfer from bacteria to eukaryotes. Nature Reviews Microbiology 16, 6779.
Indergand, S and Graf, J (2000) Ingested blood contributes to the specificity of the symbiosis of Aeromonas veronii biovar sobria and Hirudo medicinalis, the medicinal leech. Applied and Environmental Microbiology 66, 47354741.
International Glossina Genome Initiative (2014) Genome sequence of the tsetse fly (Glossina morsitans): vector of African trypanosomiasis. Science 344, 380386.
Kelly, PH, et al. (2017) The gut microbiome of the vector Lutzomyia longipalpis is essential for survival of Leishmania infantum. mBio 8, e0112116.
Kikuchi, Y, et al. (2009) Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs. BMC Biology 7, 2.
Kim, JH, et al. (2011) Comparison of the humoral and cellular immune responses between body and head lice following bacterial challenge. Insect Biochemistry and Molecular Biology 41, 332339.
Kirkness, EF, et al. (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proceedings of the National Academy of Sciences of the USA 107, 1216812173.
Klasson, L, et al. (2009) Horizontal gene transfer between Wolbachia and the mosquito Aedes aegypti. BMC Genomics 10, 33.
Kumar, S, et al. (2010) A peroxidase/dual oxidase system modulates midgut epithelial immunity in Anopheles gambiae. Science 327, 16441648.
Kwong, WK and Moran, NA (2016) Gut microbial communities of social bees. Nature Reviews Microbiology 14, 374384.
Langer, RC and Vinetz, JM (2001) Plasmodium ookinete-secreted chitinase and parasite penetration of the mosquito peritrophic matrix. Trends in Parasitology 17, 269272.
Lawrence, AL, et al. (2015) Evaluation of the bacterial microbiome of two flea species using different DNA-isolation techniques provides insights into flea host ecology. FEMS Microbiology Ecology 91, fiv134.
Lehane, MJ (1997) Peritrophic matrix structure and function. Annual Review of Entomology 42, 525550.
Lehane, MJ (2005) The Biology of Blood-Sucking in Insects. Cambridge, UK: Cambridge University Press. doi: 10.1017/CBO9780511610493.
Lo, W-S and Kuo, C-H (2017) Horizontal acquisition and transcriptional integration of novel genes in mosquito-associated Spiroplasma. Genome Biology and Evolution 9, 32463259.
Login, FH, et al. (2011) Antimicrobial peptides keep insect endosymbionts under control. Science 334, 362365.
Luan, J-B, et al. (2015) Metabolic coevolution in the bacterial symbiosis of whiteflies and related plant sap-feeding insects. Genome Biology and Evolution 7, 26352647.
Maltz, MA, et al. (2012) OmpA-mediated biofilm formation is essential for the commensal bacterium Sodalis glossinidius to colonize the tsetse fly gut. Applied and Environmental Microbiology 78, 77607768.
Mans, BJ and Neitz, AWH (2004) Adaptation of ticks to a blood-feeding environment: evolution from a functional perspective. Insect Biochemistry and Molecular Biology 34, 117.
Manzano-Marin, A, et al. (2015) Solving a bloody mess: B-vitamin independent metabolic convergence among gamma proteobacterial obligate endosymbionts from blood-feeding arthropods and the leech Haementeria officinalis. Genome Biology and Evolution 7, 28712884.
Maslov, DA, et al. (2013) Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. Trends in Parasitology 29, 4352.
McCutcheon, JP and Moran, NA (2011) Extreme genome reduction in symbiotic bacteria. Nature Reviews Microbiology 10, 1326.
Mesquita, RD, et al. (2015) Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. Proceedings of the National Academy of Sciences 112, 49364941.
Michalkova, V, et al. (2014) Obligate symbiont-generated vitamin B6 is critical to maintain proline homeostasis and fecundity in tsetse flies. Applied and Environmental Microbiology 80, 58445853.
Minard, G, Mavingui, P and Moro, CV (2013) Diversity and function of bacterial microbiota in the mosquito holobiont. Parasites & Vectors 6, 146.
Moliner, C, Fournier, P-EE and Raoult, D (2010) Genome analysis of microorganisms living in amoebae reveals a melting pot of evolution. FEMS Microbiology Reviews 34, 281294.
Moran, NA and Bennett, GM (2014) The tiniest tiny genomes. Annual Review of Microbiology 68, 195215.
Moran, NA, McCutcheon, JP and Nakabachi, A (2008) Genomics and evolution of heritable bacterial symbionts. Annual Review of Genetics 42, 165190.
Morrison, DA (2009) Evolution of the Apicomplexa: where are we now? Trends in Parasitology 25, 375382.
Morse, SF, et al. (2013) Evolution, multiple acquisition, and localization of endosymbionts in bat flies (Diptera: Hippoboscoidea: Streblidae and Nycteribiidae). Applied and Environmental Microbiology 79, 29522961.
Moses, AS, et al. (2017) Horizontally acquired biosynthesis genes boost Coxiella burnetii’s physiology. Frontiers in Cellular and Infection Microbiology 7, 174.
Nikoh, N, et al. (2014) Evolutionary origin of insect-Wolbachia nutritional mutualism. Proceedings of the National Academy of Sciences 111, 1025710262.
Nováková, E, et al. (2015) Arsenophonus and Sodalis symbionts in louse flies: an analogy to the Wigglesworthia and Sodalis system in tsetse flies. Applied and Environmental Microbiology 81, 61896199.
Nováková, E, et al. (2016) Genome sequence of Candidatus Arsenophonus lipopteni, the exclusive symbiont of a blood sucking fly Lipoptena cervi (Diptera: Hippoboscidae). Standards in Genomic Sciences 11, 72.
Pachebat, JA, et al. (2013) Draft genome sequence of Rhodococcus rhodnii strain LMG5362, a symbiont of Rhodnius prolixus (Hemiptera, Reduviidae, Triatominae), the principle vector of Trypanosoma cruzi. Genome Announcements 1, 34.
Pais, R, et al. (2008) The obligate mutualist Wigglesworthia glossinidia influences reproduction, digestion, and immunity processes of its host, the tsetse fly. Applied and Environmental Microbiology 74, 59655974.
Palavesam, A, et al. (2012) Pyrosequencing-based analysis of the microbiome associated with the horn fly, Haematobia irritans. PLoS ONE 7, e44390.
Pontes, MH, et al. (2008) Quorum sensing primes the oxidative stress response in the insect endosymbiont, Sodalis glossinidius. PLoS ONE 3, e3541.
Puchta, O (1954) Experimentelle untersuchungen uber die symbiose der kleiderlaus Pediculus vestimenti Burm. Naturwissenschaften 41, 7172.
Puchta, O (1955) Experimentelle untersuchungen uber die bedeutung der symbiose der kleiderlaus Pediculus vestimenti Burm. Zeitschrift Fur Parasitenkunde 17, 140.
Ribeiro, JMC and Francischetti, IMB (2003) Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annual Review of Entomology 48, 7388.
Richmond, GS and Smith, TK (2007) A novel phospholipase from Trypanosoma brucei. Molecular Microbiology 63, 10781095.
Ries, E (1931) Die symbiose der laüse und federlinge. Zeitschrift für Morphologie und Ökologie der Tiere 20, 233367.
Říhová, J, et al. (2017) Legionella becoming a mutualist: adaptive processes shaping the genome of symbiont in the louse Polyplax serrata. Genome Biology and Evolution 9, 29462957.
Rio, RV, et al. (2012) Insight into the transmission biology and species-specific functional capabilities of tsetse (Diptera: Glossinidae) obligate symbiont Wigglesworthia. mBio 3, 113.
Rio, RVM, Attardo, GM and Weiss, BL (2016) Grandeur alliances: symbiont metabolic integration and obligate arthropod hematophagy. Trends in Parasitology 32, 739749.
Rose, C, et al. (2014) An investigation into the protein composition of the teneral Glossina morsitans morsitans peritrophic matrix. PLoS Neglected Tropical Diseases 8, e2691.
Rosenfeld, JA, et al. (2016) Genome assembly and geospatial phylogenomics of the bed bug Cimex lectularius. Nature Communications 7, 10164.
Ross, BD, et al. (2017). Ixodes scapularis does not harbor a stable midgut microbiome. bioRxiv 198267. doi: 10.1101/198267.
Salem, H, et al. (2017) Drastic genome reduction in an herbivore's pectinolytic symbiont. Cell 171, 15201531.
Sasaki-Fukatsu, K, et al. (2006) Symbiotic bacteria associated with stomach discs of human lice. Applied and Environmental Microbiology 72, 73497352.
Sateriale, A and Striepen, B (2016) Beg, borrow and steal: three aspects of horizontal gene transfer in the protozoan parasite, Cryptosporidium parvum. PLoS Pathogens 12, e1005429.
Schluter, D and Grant, PR (1984) Ecological correlates of morphological evolution in a Darwin's finch, Geospiza difficilis. Evolution 38, 856869.
Schoeler, GB and Wikel, SK (2001) Modulation of host immunity by haematophagous arthropods. Annals of Tropical Medicine and Parasitology 95, 755771.
Schwarz, EM, et al. (2015) The genome and transcriptome of the zoonotic hookworm Ancylostoma ceylanicum identify infection-specific gene families. Nature Genetics 47, 416422.
Shao, L, Devenport, M and Jacobs-Lorena, M (2001) The peritrophic matrix of hematophagous insects. Archives of Insect Biochemistry and Physiology 47, 119125.
Sloan, DB, et al. (2014) Parallel histories of horizontal gene transfer facilitated extreme reduction of endosymbiont genomes in sap-feeding insects. Molecular Biology and Evolution 31, 857871.
Smith, TA, et al. (2015) A Coxiella-like endosymbiont is a potential vitamin source for the Lone Star tick. Genome Biology and Evolution 7, 831838.
Šochová, E, et al. (2017) Arsenophonus and Sodalis replacements shape evolution of symbiosis in louse flies. PeerJ 5, e4099.
Sojka, D, et al. (2013) New insights into the machinery of blood digestion by ticks. Trends in Parasitology 29, 276285.
Takken, W and Verhulst, NO (2013) Host preferences of blood-feeding mosquitoes. Annual Review of Entomology 58, 433453.
Tetlock, A, et al. (2012) Changes in the gut microbiome of the sea lamprey during metamorphosis. Applied and Environmental Microbiology 78, 76387644.
Vávra, J and Lukeš, J (2013) Microsporidia and ‘the art of living together’. Advances in Parasitology 82, 253319, doi: 10.1016/B978-0-12-407706-5.00004-6.
Wang, JW and Aksoy, S (2012) PGRP-LB is a maternally transmitted immune milk protein that influences symbiosis and parasitism in tsetse's offspring. Proceedings of the National Academy of Sciences 109, 1055210557.
Wang, JW, et al. (2009) Interactions between mutualist Wigglesworthia and tsetse peptidoglycan recognition protein (PGRP-LB) influence trypanosome transmission. Proceedings of the National Academy of Sciences of the USA 106, 1213312138.
Wang, S, et al. (2017) Driving mosquito refractoriness to Plasmodium falciparum with engineered symbiotic bacteria. Science 357, 13991402.
Weiss, B and Aksoy, S (2011) Microbiome influences on insect host vector competence. Trends in Parasitology 27, 514522.
Weiss, BL, et al. (2008) An insect symbiosis is influenced by bacterium-specific polymorphisms in outer-membrane protein A. Proceedings of the National Academy of Sciences of the USA 105, 1508815093.
Weiss, BL, Wang, J and Aksoy, S (2011) Tsetse immune system maturation requires the presence of obligate symbionts in larvae. PLoS Biology 9, e1000619.
Weiss, BLB, Maltz, M and Aksoy, S (2012) Obligate symbionts activate immune system development in the tsetse fly. The Journal of Immunology 188, 33953403.
Weiss, BL, et al. (2013) Trypanosome infection establishment in the tsetse fly gut is influenced by microbiome-regulated host immune barriers. PLoS Pathogens 9, e1003318.
Wigglesworth, VB (1929) Digestion in the tsetse-fly: a study of structure and function. Parasitology 21, 288321.
Wigglesworth, VB (1936) Symbiotic bacteria in a blood-sucking insect, Rhodnius prolixus Stål. (Hemiptera, Triatomidae). Parasitology 28, 284289.
Williamson, AL, et al. (2003) Digestive proteases of blood-feeding nematodes. Trends in Parasitology 19, 417423.
Woolfit, M, et al. (2009) An ancient horizontal gene transfer between mosquito and the endosymbiotic bacterium Wolbachia pipientis. Molecular Biology and Evolution 26, 367374.
Wu, B, et al. (2013) Interdomain lateral gene transfer of an essential ferrochelatase gene in human parasitic nematodes. Proceedings of the National Academy of Sciences of the USA 110, 77487753.
Zhou, G, Pennington, JE and Wells, MA (2004) Utilization of pre-existing energy stores of female Aedes aegypti mosquitoes during the first gonotrophic cycle. Insect Biochemistry and Molecular Biology 34(9), 919925.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 30
Total number of PDF views: 133 *
Loading metrics...

Abstract views

Total abstract views: 678 *
Loading metrics...

* Views captured on Cambridge Core between 12th April 2018 - 22nd September 2018. This data will be updated every 24 hours.