Interactions of the Intracellular Bacterium Cardinium with Its Host, the House Dust Mite Dermatophagoides farinae, Based on Gene Expression Data
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články
Grantová podpora
19-09998S
Grantová Agentura České Republiky (GAČR)
RO0418
Ministerstvo Zemědělství (Ministry of Agriculture)
19-14-00004
Russian Science Foundation (RSF)
PubMed
34726490
PubMed Central
PMC8562489
DOI
10.1128/msystems.00916-21
Knihovny.cz E-zdroje
- Klíčová slova
- Cardinium, allergens, endosymbiont, host-pathogen interactions, house dust mite, interactions, symbiont, transcriptome,
- Publikační typ
- časopisecké články MeSH
Dermatophagoides farinae is inhabited by an intracellular bacterium, Cardinium. Using correlations between host and symbiont gene expression profiles, we identified several important molecular pathways that potentially regulate/facilitate their interactions. The expression of Cardinium genes collectively explained 95% of the variation in the expression of mite genes assigned to pathways for phagocytosis, apoptosis, the MAPK signaling cascade, endocytosis, the tumor necrosis factor (TNF) pathway, the transforming growth factor beta (TGF-β) pathway, lysozyme, and the Toll/Imd pathway. In addition, expression of mite genes explained 76% of the variability in Cardinium gene expression. In particular, the expression of the Cardinium genes encoding the signaling molecules BamD, LepA, SymE, and VirD4 was either positively or negatively correlated with the expression levels of mite genes involved in endocytosis, phagocytosis, and apoptosis. We also found that Cardinium possesses a complete biosynthetic pathway for lipoic acid and may provide lipoate, but not biotin, to mites. Cardinium gene expression collectively explained 84% of the variation in expression related to several core mite metabolic pathways, and, most notably, a negative correlation was observed between bacterial gene expression and expression of mite genes assigned to the glycolysis and citric acid cycle pathways. Furthermore, we showed that Cardinium gene expression is correlated with expression levels of genes associated with terpenoid backbone biosynthesis. This pathway is important for the synthesis of pheromones, thus providing an opportunity for Cardinium to influence mite reproductive behavior to facilitate transmission of the bacterium. Overall, our study provided correlational gene expression data that can be useful for future research on mite-Cardinium interactions. IMPORTANCE The molecular mechanisms of mite-symbiont interactions and their impacts on human health are largely unknown. Astigmatid mites, such as house dust and stored-product mites, are among the most significant allergen sources worldwide. Although mites themselves are the main allergen sources, recent studies have indicated that mite-associated microbiomes may have implications for allergen production and human health. The major medically important house dust mite, D. farinae, is known to harbor a highly abundant intracellular bacterium belonging to the genus Cardinium. Expression analysis of the mite and symbiont genes can identify key mite molecular pathways that facilitate interactions with this endosymbiont and possibly shed light on how this bacterium affects mite allergen production and physiology in general.
Crop Research Institute Prague Czechia
Faculty of Biology Tyumen State University Tyumen Russia
School of Natural Sciences Bangor University Bangor United Kingdom
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Ju J-F, Bing X-L, Zhao D-S, Guo Y, Xi Z, Hoffmann AA, Zhang K-J, Huang H-J, Gong J-T, Xu Zhang X, Hong X-Y. 2020. PubMed DOI PMC
Ren F-R, Sun X, Wang T-Y, Yao Y-L, Huang Y-Z, Zhang X, Luan J-B. 2020. Biotin provisioning by horizontally transferred genes from bacteria confers animal fitness benefits. ISME J 14:2542–2553. doi: 10.1038/s41396-020-0704-5. PubMed DOI PMC
Husnik F, Hypsa V, Darby A. 2020. Insect-symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite. Genome Biol Evol 12:429–442. doi: 10.1093/gbe/evaa032. PubMed DOI PMC
Zhu Y-X, Song Z-R, Song Y-L, Hong X-Y. 2020. Double infection of PubMed DOI
Brown AMV, Wasala SK, Howe DK, Peetz AB, Zasada IA, Denver DR. 2018. Comparative genomics of PubMed DOI PMC
Siozios S, Pilgrim J, Darby AC, Baylis M, Hurst GDD. 2019. The draft genome of strain PubMed DOI PMC
Morag N, Klement E, Saroya Y, Lensky I, Gottlieb Y. 2012. Prevalence of the symbiont PubMed DOI
Chang J, Masters A, Avery A, Werren JH. 2010. A divergent PubMed DOI
Duron O, Hurst GDD, Hornett EA, Josling JA, Engelstadter J. 2008. High incidence of the maternally inherited bacterium PubMed DOI
Chigira A, Miura K. 2005. Detection of ‘ PubMed DOI
Penz T, Schmitz-Esser S, Kelly SE, Cass BN, Muller A, Woyke T, Malfatti SA, Hunter MS, Horn M. 2012. Comparative genomics suggests an independent origin of cytoplasmic incompatibility in PubMed DOI PMC
Colloff MJ. 2009. Dust mites. CSIRO Publishing, Collingwood, VIC, Australia.
Spieksma FTM. 1997. Domestic mites from an acarologic perspective. Allergy 52:360–368. doi: 10.1111/j.1398-9995.1997.tb01012.x. PubMed DOI
OConnor BM. 1979. Evolutionary origins of astigmatid mites inhabiting stored products, p 273–278. DOI
WHO/IUIS Allergen Nomenclature Sub-Committee. 2020. Allergen nomenclature. Astigmata. WHO/IUIS Allergen Nomenclature Sub-Committee. http://www.allergen.org/search.php?TaxOrder=Astigmata.
Kim JY, Yi M-H, Hwang Y, Lee JY, Lee I-Y, Yong D, Yong T-S. 2018. 16S rRNA profiling of the PubMed DOI
Lee J, Kim JY, Yi M-h, Hwang Y, Lee I-Y, Nam S-H, Yong D, Yong T-S. 2019. Comparative microbiome analysis of PubMed DOI
Valerio CR, Murray P, Arlian LG, Slater JE. 2005. Bacterial 16S ribosomal DNA in house dust mite cultures. J Allergy Clin Immunol 116:1296–1300. doi: 10.1016/j.jaci.2005.09.046. PubMed DOI
Hubert J, Nesvorna M, Klimov P, Dowd SE, Sopko B, Erban T. 2019. Differential allergen expression in three PubMed DOI
Dzoro S, Mittermann I, Resch-Marat Y, Vrtala S, Nehr M, Hirschl AM, Wikberg G, Lundeberg L, Johansson C, Scheynius A, Valenta R. 2018. House dust mites as potential carriers for IgE sensitization to bacterial antigens. Allergy 73:115–124. doi: 10.1111/all.13260. PubMed DOI PMC
Erban T, Hubert J. 2008. Digestive function of lysozyme in synanthropic acaridid mites enables utilization of bacteria as a food source. Exp Appl Acarol 44:199–212. doi: 10.1007/s10493-008-9138-x. PubMed DOI
Hubert J, Nesvorna M, Kopecky J, Erban T, Klimov P. 2019. Population and culture age influence the microbiome profiles of house dust mites. Microb Ecol 77:1048–1066. doi: 10.1007/s00248-018-1294-x. PubMed DOI
Klimov P, Molva V, Nesvorna M, Pekar S, Shcherbachenko E, Erban T, Hubert J. 2019. Dynamics of the microbial community during growth of the house dust mite PubMed DOI
Nakamura Y, Kawai S, Yukuhiro F, Ito S, Gotoh T, Kisimoto R, Yanase T, Matsumoto Y, Kageyama D, Noda H. 2009. Prevalence of PubMed DOI PMC
Erban T, Klimov P, Molva V, Hubert J. 2020. Whole genomic sequencing and sex-dependent abundance estimation of PubMed DOI
Kitajima EW, Groot TVM, Novelli VM, Freitas-Astua J, Alberti G, de Moraes GJ. 2007. PubMed DOI
Hubert J, Kopecky J, Perotti MA, Nesvorna M, Braig HR, Sagova-Mareckova M, Macovei L, Zurek L. 2012. Detection and identification of species-specific bacteria associated with synanthropic mites. Microb Ecol 63:919–928. doi: 10.1007/s00248-011-9969-6. PubMed DOI
Trivedi B, Valerio C, Slater JE. 2003. Endotoxin content of standardized allergen vaccines. J Allergy Clin Immunol 111:777–783. doi: 10.1067/mai.2003.1338. PubMed DOI
Valerio C, Murray P, Arlian LG, Slater JE. 2004. Endotoxin in dust mite allergen extracts. J Allergy Clin Immunol 113:S136–S137. doi: 10.1016/j.jaci.2003.12.489. DOI
Valerio C, Arlian LG, Slater JE. 2009. Bacterial DNA sequences isolated from standardized dust mite extracts and wild mites. J Allergy Clin Immunol 123:S216–S216. doi: 10.1016/j.jaci.2008.12.826. DOI
Kim JY, Yi M, Lee J, Lee I, Yong T. 2019. Potential immunomodulatory effect of the house dust mite microbiome. Allergy 74:LBTP1825.
Smith TE, Moran NA. 2020. Coordination of host and symbiont gene expression reveals a metabolic tug-of-war between aphids and PubMed DOI PMC
Mann E, Stouthamer CM, Kelly SE, Dzieciol M, Hunter MS, Schmitz-Esser S. 2017. Transcriptome sequencing reveals novel candidate genes for PubMed DOI PMC
Li C, He M, Yun Y, Peng Y. 2020. Co-infection with PubMed DOI
Martinez-Giron R, Doganci L, Iraola V. 2009. Gregarines in PubMed DOI
Martinez-Giron R. 2018. Flagellated protozoa detected in PubMed DOI
Ribas A, Martinez-Giron R. 2006. Protozoal forms in house-dust mites and respiratory allergy. Allergy Asthma Proc 27:347–349. doi: 10.2500/aap.2006.27.2878. PubMed DOI
Larsson JIR, Steiner MY, Bjornson S. 1997.
Andersen A. 1991. Nutritional value of yeast for PubMed DOI
Eraso E, Martinez J, Garcia-Ortega P, Martinez A, Palacios R, Cisterna R, Guisantes JA. 1998. Influence of mite growth culture phases on the biological standardization of allergenic extracts. J Invest Allergol Clin Immunol 8:201–206. PubMed
Eraso E, Martinez J, Martinez A, Palacios R, Guisantes JA. 1997. Quality parameters for the production of mite extracts. Allergol Immunopathol (Madr) 25:113–117. PubMed
Eraso E, Guisantes JA, Martinez J, Saenz-de-Santamaria M, Martinez A, Palacios R, Cisterna R. 1997. Kinetics of allergen expression in cultures of house dust mites, PubMed DOI
Kremer N, Charif D, Henri H, Gavory F, Wincker P, Mavingui P, Vavre F. 2012. Influence of PubMed DOI PMC
Herbert RI, McGraw EA. 2018. The nature of the immune response in novel DOI
Pan X, Pike A, Joshi D, Bian G, McFadden MJ, Lu P, Liang X, Zhang F, Raikhel AS, Xi Z. 2018. The bacterium PubMed DOI PMC
Surachetpong W, Singh N, Cheung KW, Luckhart S. 2009. MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to PubMed DOI PMC
Patrnogic J, Heryanto C, Eleftherianos I. 2018. Transcriptional up-regulation of the TGF-beta intracellular signaling transducer Mad of PubMed DOI PMC
Kawasaki T, Kawai T. 2014. Toll-like receptor signaling pathways. Front Immunol 5:461. doi: 10.3389/fimmu.2014.00461. PubMed DOI PMC
Varfolomeev EE, Ashkenazi A. 2004. Tumor necrosis factor: an apoptosis JuNKie? Cell 116:491–497. doi: 10.1016/S0092-8674(04)00166-7. PubMed DOI
Waldron R, McGowan J, Gordon N, McCarthy C, Mitchell EB, Doyle S, Fitzpatrick DA. 2017. Draft genome sequence of PubMed DOI PMC
Salzet M. 2001. Vertebrate innate immunity resembles a mosaic of invertebrate immune responses. Trends Immunol 22:285–288. doi: 10.1016/S1471-4906(01)01895-6. PubMed DOI
Imler J-L, Zheng L. 2004. Biology of Toll receptors: lessons from insects and mammals. J Leukoc Biol 75:18–26. doi: 10.1189/jlb.0403160. PubMed DOI
Zheng L, Zhang L, Lin H, McIntosh MT, Malacrida A. 2005. Toll-like receptors in invertebrate innate immunity. Invertebr Surviv J 2:105–113.
Coscia MR, Giacomelli S, Oreste U. 2011. Toll-like receptors: an overview from invertebrates to vertebrates. Invertebr Surviv J 8:210–226.
Zychlinsky A, Sansonetti P. 1997. Perspectives series: host/pathogen interactions. Apoptosis in bacterial pathogenesis. J Clin Invest 100:493–495. doi: 10.1172/JCI119557. PubMed DOI PMC
Zhukova MV, Kiseleva E. 2012. The virulent PubMed DOI PMC
Guo Y, Hoffmann AA, Xu X-Q, Zhang X, Huang H-J, Ju J-F, Gong J-T, Hong X-Y. 2018. PubMed DOI
Almeida F, Suesdek L. 2017. Effects of PubMed DOI PMC
Lu H-l, Chang C-c, Wilson ACC. 2016. Amino acid transporters implicated in endocytosis of PubMed DOI PMC
Koga R, Meng X-Y, Tsuchida T, Fukatsu T. 2012. Cellular mechanism for selective vertical transmission of an obligate insect symbiont at the bacteriocyte-embryo interface. Proc Natl Acad Sci USA 109:E1230–E1237. doi: 10.1073/pnas.1119212109. PubMed DOI PMC
White PM, Pietri JE, Debec A, Russell S, Patel B, Sullivan W. 2017. Mechanisms of horizontal cell-to-cell transfer of PubMed DOI PMC
Fattouh N, Cazevieille C, Landmann F. 2019. PubMed DOI PMC
Gerardo NM, Hoang KL, Stoy KS. 2020. Evolution of animal immunity in the light of beneficial symbioses. Philos Trans R Soc Lond B Biol Sci 375:20190601. doi: 10.1098/rstb.2019.0601. PubMed DOI PMC
Chang Z. 2016. The function of the DegP (HtrA) protein: protease versus chaperone. IUBMB Life 68:904–907. doi: 10.1002/iub.1561. PubMed DOI
Kuykendall LD, Shao JY, Hartung JS. 2012. ‘ PubMed DOI PMC
Chi X, Fan Q, Zhang Y, Liang K, Wan L, Zhou Q, Li Y. 2020. Structural mechanism of phospholipids translocation by MlaFEDB complex. Cell Res 30:1127–1135. doi: 10.1038/s41422-020-00404-6. PubMed DOI PMC
Doyle MT, Bernstein HD. 2019. Bacterial outer membrane proteins assemble via asymmetric interactions with the BamA β-barrel. Nat Commun 10:3358. doi: 10.1038/s41467-019-11230-9. PubMed DOI PMC
Bowyer A, Baardsnes J, Ajamian E, Zhang L, Cygler M. 2011. Characterization of interactions between LPS transport proteins of the Lpt system. Biochem Biophys Res Commun 404:1093–1098. doi: 10.1016/j.bbrc.2010.12.121. PubMed DOI
Ayala-Castro C, Saini A, Outten FW. 2008. Fe-S cluster assembly pathways in bacteria. Microbiol Mol Biol Rev 72:110–125. doi: 10.1128/MMBR.00034-07. PubMed DOI PMC
Backert S, Meyer TF. 2006. Type IV secretion systems and their effectors in bacterial pathogenesis. Curr Opin Microbiol 9:207–217. doi: 10.1016/j.mib.2006.02.008. PubMed DOI
Best AM, Abu Kwaik Y. 2019. Evasion of phagotrophic predation by protist hosts and innate immunity of metazoan hosts by PubMed DOI PMC
Flieger A, Frischknecht F, Hacker G, Hornef MW, Pradel G. 2018. Pathways of host cell exit by intracellular pathogens. Microb Cell 5:525–544. doi: 10.15698/mic2018.12.659. PubMed DOI PMC
Hunt TP, Magasanik B. 1985. Transcription of PubMed DOI PMC
Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M. 2010. The genome of the amoeba symbiont “ PubMed DOI PMC
Rosas-Perez T, Rosenblueth M, Rincon-Rosales R, Mora J, Martinez-Romero E. 2014. Genome sequence of “ PubMed DOI PMC
Kambhampati S, Alleman A, Park Y. 2013. Complete genome sequence of the endosymbiont PubMed DOI
Toh H, Weiss BL, Perkin SAH, Yamashita A, Oshima K, Hattori M, Aksoy S. 2006. Massive genome erosion and functional adaptations provide insights into the symbiotic lifestyle of PubMed DOI PMC
Showmaker KC, Walden KKO, Fields CJ, Lambert KN, Hudson ME. 2018. Genome sequence of the soybean cyst nematode ( PubMed DOI PMC
Zeng Z, Fu Y, Guo D, Wu Y, Ajayi OE, Wu Q. 2018. Bacterial endosymbiont PubMed DOI PMC
Fronzes R, Christie PJ, Waksman G. 2009. The structural biology of type IV secretion systems. Nat Rev Microbiol 7:703–714. doi: 10.1038/nrmicro2218. PubMed DOI PMC
Heddi A, Grenier A-M, Khatchadourian C, Charles H, Nardon P. 1999. Four intracellular genomes direct weevil biology: nuclear, mitochondrial, principal endosymbiont, and PubMed DOI PMC
Heddi A, Lefebvre F, Nardon P. 1993. Effect of endocytobiotic bacteria on mitochondrial enzymatic activities in the weevil DOI
Douglas AE. 1998. Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria PubMed DOI
Dale C, Moran NA. 2006. Molecular interactions between bacterial symbionts and their hosts. Cell 126:453–465. doi: 10.1016/j.cell.2006.07.014. PubMed DOI
Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of PubMed DOI
Ankrah NYD, Chouaia B, Douglas AE. 2018. The cost of metabolic interactions in symbioses between insects and bacteria with reduced genomes. mBio 9:e01433-18. doi: 10.1128/mBio.01433-18. PubMed DOI PMC
McCutcheon JP, Moran NA. 2010. Functional convergence in reduced genomes of bacterial symbionts spanning 200 My of evolution. Genome Biol Evol 2:708–718. doi: 10.1093/gbe/evq055. PubMed DOI PMC
Gupta A, Nair S. 2020. Dynamics of insect-microbiome interaction influence host and microbial symbiont. Front Microbiol 11:1357. doi: 10.3389/fmicb.2020.01357. PubMed DOI PMC
Santos-Garcia D, Rollat-Farnier P-A, Beitia F, Zchori-Fein E, Vavre F, Mouton L, Moya A, Latorre A, Silva FJ. 2014. The genome of PubMed DOI PMC
Wada-Katsumata A, Zurek L, Nalyanya G, Roelofs WL, Zhang A, Schal C. 2015. Gut bacteria mediate aggregation in the German cockroach. Proc Natl Acad Sci USA 112:15678–15683. doi: 10.1073/pnas.1504031112. PubMed DOI PMC
Van Arnam EB, Currie CR, Clardy J. 2018. Defense contracts: molecular protection in insect-microbe symbioses. Chem Soc Rev 47:1638–1651. doi: 10.1039/c7cs00340d. PubMed DOI
Becerra JX, Venable GX, Saeidi V. 2015. PubMed DOI
Brody AR, Wharton GW. 1970. PubMed DOI
Raspotnig G. 2010. Oil gland secretions in Oribatida (Acari), p 235–239. DOI
Vandermoten S, Mescher MC, Francis F, Haubruge E, Verheggen FJ. 2012. Aphid alarm pheromone: an overview of current knowledge on biosynthesis and functions. Insect Biochem Mol Biol 42:155–163. doi: 10.1016/j.ibmb.2011.11.008. PubMed DOI
Hojo M, Matsumoto T, Miura T. 2007. Cloning and expression of a geranylgeranyl diphosphate synthase gene: insights into the synthesis of termite defence secretion. Insect Mol Biol 16:121–131. doi: 10.1111/j.1365-2583.2007.00709.x. PubMed DOI
Steidle JLM, Barcari E, Hradecky M, Trefz S, Tolasch T, Gantert C, Schulz S. 2014. Pheromonal communication in the European house dust mite, PubMed DOI PMC
Tatami K, Mori N, Nishida R, Kuwahara Y. 2001. 2-Hydroxy-6-methylbenzaldehyde: the female sex pheromone of the house dust mite DOI
Kuwahara Y, Leal WS, Suzuki T. 1990. Pheromone study on astigmatid mites XXVI. Comparison of volatile components between DOI
Konakandla B, Park Y, Margolies D. 2006. Whole genome amplification of Chelex-extracted DNA from a single mite: a method for studying genetics of the predatory mite PubMed DOI
Hubert J, Erban T, Kopecky J, Sopko B, Nesvorna M, Lichovnikova M, Schicht S, Strube C, Sparagano O. 2017. Comparison of microbiomes between red poultry mite populations ( PubMed DOI
Seemann T. 2014. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069. doi: 10.1093/bioinformatics/btu153. PubMed DOI
Cuccuru G, Orsini M, Pinna A, Sbardellati A, Soranzo N, Travaglione A, Uva P, Zanetti G, Fotia G. 2014. Orione, a web-based framework for NGS analysis in microbiology. Bioinformatics 30:1928–1929. doi: 10.1093/bioinformatics/btu135. PubMed DOI PMC
Afgan E, Baker D, Batut B, van den Beek M, Bouvier D, Cech M, Chilton J, Clements D, Coraor N, Gruning BA, Guerler A, Hillman-Jackson J, Hiltemann S, Jalili V, Rasche H, Soranzo N, Goecks J, Taylor J, Nekrutenko A, Blankenberg D. 2018. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update. Nucleic Acids Res 46:W537–W544. doi: 10.1093/nar/gky379. PubMed DOI PMC
Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R, Beeman RW, Brown SJ, Bucher G, Friedrich M, Grimmelikhuijzen CJ, Klingler M, Lorenzen M, Richards S, Roth S, Schroder R, Tautz D, Zdobnov EM, Muzny D, Gibbs RA, Weinstock GM, Attaway T, Bell S, Buhay CJ, Chandrabose MN, Chavez D, Clerk-Blankenburg KP, Cree A, Dao M, Davis C, Chacko J, Dinh H, Dugan-Rocha S, Fowler G, Garner TT, Garnes J, Gnirke A, Hawes A, Hernandez J, Hines S, Holder M, Hume J, Jhangiani SN, Joshi V, Khan ZM, Jackson L, Kovar C, Kowis A, Lee S, Tribolium Genome Sequencing Consortium , et al. 2008. The genome of the model beetle and pest PubMed DOI
Rider SD, Jr, Morgan MS, Arlian LG. 2015. Draft genome of the scabies mite. Parasit Vectors 8:585. doi: 10.1186/s13071-015-1198-2. PubMed DOI PMC
Grbic M, Van Leeuwen T, Clark RM, Rombauts S, Rouze P, Grbic V, Osborne EJ, Dermauw W, Ngoc PC, Ortego F, Hernandez-Crespo P, Diaz I, Martinez M, Navajas M, Sucena E, Magalhaes S, Nagy L, Pace RM, Djuranovic S, Smagghe G, Iga M, Christiaens O, Veenstra JA, Ewer J, Villalobos RM, Hutter JL, Hudson SD, Velez M, Yi SV, Zeng J, Pires-daSilva A, Roch F, Cazaux M, Navarro M, Zhurov V, Acevedo G, Bjelica A, Fawcett JA, Bonnet E, Martens C, Baele G, Wissler L, Sanchez-Rodriguez A, Tirry L, Blais C, Demeestere K, Henz SR, Gregory TR, Mathieu J, Verdon L, Farinelli L, Schmutz J, Lindquist E, et al. 2011. The genome of PubMed DOI PMC
Zajc J, Liu Y, Dai W, Yang Z, Hu J, Gostincar C, Gunde-Cimerman N. 2013. Genome and transcriptome sequencing of the halophilic fungus PubMed DOI PMC
Muzzey D, Schwartz K, Weissman JS, Sherlock G. 2013. Assembly of a phased diploid PubMed DOI PMC
Stromsten NJ, Benson SD, Burnett RM, Bamford DH, Bamford JKH. 2003. The PubMed DOI PMC
Segers FHID, Kesnerova L, Kosoy M, Engel P. 2017. Genomic changes associated with the evolutionary transition of an insect gut symbiont into a blood-borne pathogen. ISME J 11:1232–1244. doi: 10.1038/ismej.2016.201. PubMed DOI PMC
Kosoy M, Morway C, Sheff KW, Bai Y, Colborn J, Chalcraft L, Dowell SF, Peruski LF, Maloney SA, Baggett H, Sutthirattana S, Sidhirat A, Maruyama S, Kabeya H, Chomel BB, Kasten R, Popov V, Robinson J, Kruglov A, Petersen LR. 2008. PubMed DOI PMC
Tokuda G, Elbourne LDH, Kinjo Y, Saitoh S, Sabree Z, Hojo M, Yamada A, Hayashi Y, Shigenobu S, Bandi C, Paulsen IT, Watanabe H, Lo N. 2013. Maintenance of essential amino acid synthesis pathways in the PubMed DOI PMC
Koga R, Moran NA. 2014. Swapping symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont. ISME J 8:1237–1246. doi: 10.1038/ismej.2013.235. PubMed DOI PMC
Finn RD, Clements J, Eddy SR. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39:W29–W37. doi: 10.1093/nar/gkr367. PubMed DOI PMC
Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD. 2018. HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204. doi: 10.1093/nar/gky448. PubMed DOI PMC
Kanehisa M, Goto S. 2000. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28:27–30. doi: 10.1093/nar/28.1.27. PubMed DOI PMC
Hammer O, Harper DAT, Ryan PD. 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:4. https://palaeo-electronica.org/2001_1/past/issue1_01.htm.
Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol 79:5112–5120. doi: 10.1128/AEM.01043-13. PubMed DOI PMC
Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MH, Szoecs E, Wagner H. 2019. Package ‘vegan’: community ecology package, version 2.5–6. CRAN—The Comprehensive R Archive Network. https://cran.r-project.org/web/packages/vegan/vegan.pdf.
Addinsoft. 2020. XLSTAT. Addinsoft, New York, NY. https://www.xlstat.com.
jokergoo. 2020. Visualize big correlation matrix. A Bioinformagician. http://web.archive.org/web/20200424071358/http://jokergoo.github.io/blog/html/large_matrix_circular.html.
Zeleny D. 2017. Analysis of community ecology data in R: constrained ordination. https://www.davidzeleny.net/anadat-r/doku.php/en:forward_sel.
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T. 2003. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504. doi: 10.1101/gr.1239303. PubMed DOI PMC
Basu S, Duren W, Evans CR, Burant CF, Michailidis G, Karnovsky A. 2017. Sparse network modeling and Metscape-based visualization methods for the analysis of large-scale metabolomics data. Bioinformatics 33:1545–1553. doi: 10.1093/bioinformatics/btx012. PubMed DOI PMC
Genc B, Dogrusoz U. 2016. An algorithm for automated layout of process description maps drawn in SBGN. Bioinformatics 32:77–84. doi: 10.1093/bioinformatics/btv516. PubMed DOI PMC