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9. The influence of contrasting microbial lifestyles on the pre-symbiotic metabolite responses of Eucalyptus grandis roots

Author

Wong, JWH, Lutz, A, Natera, S, Wang, M, Ng, V, Grigoriev, I, Martin, F, Roessner, U, Anderson, IC, and Plett, JM

Subjects
Ecology, Evolutionary Biology
Abstract

Plant roots co-inhabit the soil with a diverse consortium of microbes of which a number attempt to enter symbiosis with the plant. These microbes may be pathogenic, mutualistic, or commensal. Hence, the health and survival of plants is heavily reliant on their ability to perceive different microbial lifestyles and respond appropriately. Emerging research suggests that there is a pivotal role for plant root secondary metabolites in responding to microbial colonization. However, it is largely unknown if plants are able to differentiate between microbes of different lifestyles and respond differently during the earliest stages of pre-symbiosis (i.e., prior to physical contact). In studying plant responses to a range of microbial isolates, we questioned: (1) if individual microbes of different lifestyles and species caused alterations to the plant root metabolome during pre-symbiosis, and (2) if these early metabolite responses correlate with the outcome of the symbiotic interaction in later phases of colonization. We compared the changes of the root tip metabolite profile of the model tree Eucalyptus grandis during pre-symbiosis with two isolates of a pathogenic fungus (Armillaria luteobubalina), one isolate of a pathogenic oomycete (Phytophthora cinnamomi), two isolates of an incompatible mutualistic fungus (Suillus granulatus), and six isolates of a compatible mutualistic fungus (Pisolithus microcarpus). Untargeted metabolite profiling revealed predominantly positive root metabolite responses at the pre-symbiosis stage, prior to any observable phenotypical changes of the root tips. Metabolite responses in the host tissue that were specific to each microbial species were identified. A deeper analysis of the root metabolomic profiles during pre-symbiotic contact with six strains of P. microcarpus showed a connection between these early metabolite responses in the root with later colonization success. Further investigation using isotopic tracing revealed a portion of metabolites found in root tips originated from the fungus. RNA-sequencing also showed that the plant roots undergo complementary transcriptomic reprogramming in response to the fungal stimuli. Taken together, our results demonstrate that the early metabolite responses of plant roots are partially selective toward the lifestyle of the interacting microbe, and that these responses can be crucial in determining the outcome of the interaction.

Published
2019

11. Comparative genomics of Mortierella elongata and its bacterial endosymbiont Mycoavidus cysteinexigens

Author

Uehling, J, Gryganskyi, A, Hameed, K, Tschaplinski, T, Misztal, PK, Wu, S, Desirò, A, Pol, N Vande, Du, Z, Zienkiewicz, A, Zienkiewicz, K, Morin, E, Tisserant, E, Splivallo, R, Hainaut, M, Henrissat, B, Ohm, R, Kuo, A, Yan, J, Lipzen, A, Nolan, M, LaButti, K, Barry, K, Goldstein, AH, Labbé, J, Schadt, C, Tuskan, G, Grigoriev, I, Martin, F, Vilgalys, R, and Bonito, G

Subjects
Microbiology, Biological Sciences, Genetics, Infectious Diseases, Human Genome, 2.2 Factors relating to the physical environment, Infection, Animals, Base Sequence, Burkholderiaceae, Carbohydrate Metabolism, Evolution, Molecular, Genome, Bacterial, Genome, Fungal, Lipid Metabolism, Metabolic Networks and Pathways, Metagenome, Mortierella, Phylogeny, Sequence Analysis, DNA, Symbiosis, Evolutionary Biology, Ecology
Abstract

Endosymbiosis of bacteria by eukaryotes is a defining feature of cellular evolution. In addition to well-known bacterial origins for mitochondria and chloroplasts, multiple origins of bacterial endosymbiosis are known within the cells of diverse animals, plants and fungi. Early-diverging lineages of terrestrial fungi harbor endosymbiotic bacteria belonging to the Burkholderiaceae. We sequenced the metagenome of the soil-inhabiting fungus Mortierella elongata and assembled the complete circular chromosome of its endosymbiont, Mycoavidus cysteinexigens, which we place within a lineage of endofungal symbionts that are sister clade to Burkholderia. The genome of M. elongata strain AG77 features a core set of primary metabolic pathways for degradation of simple carbohydrates and lipid biosynthesis, while the M. cysteinexigens (AG77) genome is reduced in size and function. Experiments using antibiotics to cure the endobacterium from the host demonstrate that the fungal host metabolism is highly modulated by presence/absence of M. cysteinexigens. Independent comparative phylogenomic analyses of fungal and bacterial genomes are consistent with an ancient origin for M. elongata - M. cysteinexigens symbiosis, most likely over 350 million years ago and concomitant with the terrestrialization of Earth and diversification of land fungi and plants.

Published
2017

13. Development of Immunoassay for Detection of Engineered Endolysin LysAm24-SMAP.

Author

Klimova, A. A., Grigoriev, I. V., Vasina, D. V., Anurova, M. N., Gushchin, V. A., and Antonova, N. P.

Subjects
*ENZYME-linked immunosorbent assay, *IMMUNOASSAY, *LYSINS, *MATRIX effect
Abstract

In recent years modified bacteriophage lysins have widely been investigated for the purposes of development of antibacterial therapy. Thus, effective and precise methods for the quantitative analysis of these enzymes are in high demand. The enzyme-linked immunosorbent assay (ELISA) method has been developed for the detection of recombinant modified endolysin LysAm24-SMAP in biological samples. The optimal parameters for protein detection were determined, in particular, the influence of salt and the composition of the buffer system for preparation of the samples was studied. The applicability of the immunodetection system of the genetically engineered endolysin LysAm24-SMAP in various biological samples with enzyme concentrations from 0.4 ng/mL was demonstrated. In addition, the influence of matrix effects in samples of animal organs and tissue homogenates and producer strain lysates and their individual components during the analysis was assessed and it was shown that 0.65 M NaCl addition in the ELISA buffer is crucial for achieving correct results and reduces nonspecific interactions in the case of LysAm24-SMAP. The effectiveness of the developed system in the immunochemical control of the bacteriolytic enzyme was confirmed. [ABSTRACT FROM AUTHOR]

Published
2024
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14. Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi

Author

Riley, R., Salamov, A. A., Brown, D. W., Nagy, L. G., Floudas, D., Held, B. W., Levasseur, A., Lombard, V., Morin, E., Otillar, R., Lindquist, E. A., Sun, H., LaButti, K. M., Schmutz, J., Jabbour, D., Luo, H., Baker, S. E., Pisabarro, A. G., Walton, J. D., Blanchette, R. A., Henrissat, B., Martin, F., Cullen, D., Hibbett, D. S., and Grigoriev, I. V.

Published
2014

18. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis

Author

Martin, F., Aerts, A., Ahren, D., Brun, A., Danchin, E. G. J., Duchaussoy, F., Gibon, J., Kohler, A., Lindquist, E., Peresa, V., Salamov, A., Shapiro, H. J., Wuyts, J., Blaudez, D., Buee, M., Brokstein, P., Canback, B., Cohen, D., Courty, P. E., Coutinho, P. M., Delaruelle, C., Detter, J. C., Deveau, A., DiFazio, S., Duplessis, S., Fraissinet-Tachet, L., Lucic, E., Frey-Klett, P., Fourrey, C., Feussner, I., Gay, G., Grimwood, J., Hoegger, P. J., Jain, P., Kilaru, S., Labbe, J., Lin, Y. C., Legue, V., Tacon, F. Le, Marmeisse, R., Melayah, D., Montanini, B., Muratet, M., Nehls, U., Niculita-Hirzel, H., Secq, M. P. Oudot-Le, Peter, M., Quesneville, H., Rajashekar, B., Reich, M., Rouhier, N., Schmutz, J., Yin, T., Chalot, M., Henrissat, B., Kues, U., Lucas, S., Peer, Y. Van de, Podila, G. K., Polle, A., Pukkila, P. J., Richardson, P. M., Rouze, P., Sanders, I. R., Stajich, J. E., Tunlid, A., Tuskan, G., and Grigoriev, I. V.

Abstract

Mycorrhizal symbioses the union of roots and soil fungi are universal in terrestrial ecosystems and may have been fundamental to land colonization by plants 1, 2. Boreal, temperate and montane forests all depend on ectomycorrhizae1. Identification of the primary factors that regulate symbiotic development and metabolic activity will therefore open the door to understanding the role of ectomycorrhizae in plant development and physiology, allowing the full ecological significance of this symbiosis to be explored. Here we report the genome sequence of the ectomycorrhizal basidiomycete Laccaria bicolor (Fig. 1) and highlight gene sets involved in rhizosphere colonization and symbiosis. This 65-megabase genome assembly contains 20,000 predicted protein-encoding genes and a very large number of transposons and repeated sequences. We detected unexpected genomic features, most notably a battery of effector-type small secreted proteins (SSPs) with unknown function, several of which are only expressed in symbiotic tissues. The most highly expressed SSP accumulates in the proliferating hyphae colonizing the host root. The ectomycorrhizae-specific SSPs probably have a decisive role in the establishment of the symbiosis. The unexpected observation that the genome of L. bicolor lacks carbohydrate-active enzymes involved in degradation of plant cell walls, but maintains the ability to degrade non-plant cell wall polysaccharides, reveals the dual saprotrophic and biotrophic lifestyle of the mycorrhizal fungus that enables it to grow within both soil and living plant roots. The predicted gene inventory of the L. bicolor genome, therefore, points to previously unknown mechanisms of symbiosis operating in biotrophic mycorrhizal fungi. The availability of this genome provides an unparalleled opportunity to develop a deeper understanding of the processes by which symbionts interact with plants within their ecosystem to perform vital functions in the carbon and nitrogen cycles that are fundamental to sustainable plant productivity.

Published
2008

19. Comparative genomics of the lactic acid bacteria

Author

Makarova, K., Slesarev, A., Wolf, Y., Sorokin, A., Mirkin, B., Koonin, E., Pavlov, A., Pavlova, N., Karamychev, V., Polouchine, N., Shakhova, V., Grigoriev, I., Lou, Y., Rokhsar, D., Lucas, S., Huang, K., Goodstein, D. M., Hawkins, T., Plengvidhya, V., Welker, D., Hughes, J., Goh, Y., Benson, A., Baldwin, K., Lee, J.-H., Diaz-Muniz, I., Dosti, B., V, Smeianov, Wechter, W., Barabote, R., Lorca, G., Altermann, E., Barrangou, R., Ganesan, B., Xie, Y., Rawsthorne, H., Tamir, D., Parker, C., Breidt, F., Broadbent, J., Hutkins, R., O'Sullivan, D., Steele, J., Unlu, G., Saier, M., Klaenhammer, T., Richardson, P., Kozyavkin, S., Weimer, B., and Mills, D.

Subjects
evolutionary genomics, fermentation
Abstract

Lactic acid-producing bacteria are associated with various plant and animal niches and play a key role in the production of fermented foods and beverages. We report nine genome sequences representing the phylogenetic and functional diversity of these bacteria. The small genomes of lactic acid bacteria encode a broad repertoire of transporters for efficient carbon and nitrogen acquisition from the nutritionally rich environments they inhabit and reflect a limited range of biosynthetic capabilities that indicate both prototrophic and auxotrophic strains. Phylogenetic analyses, comparison of gene content across the group, and reconstruction of ancestral gene sets indicate a combination of extensive gene loss and key gene acquisitions via horizontal gene transfer during the coevolution of lactic acid bacteria with their habitats.

Published
2006

20. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray)

Author

Tuskan, G.A., DiFazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R.R., Bhalerao, R.P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, G.-L., Cooper, D., Coutinho, P.M., Couturier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Dejardin, A., dePamphillis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehiting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Hamberger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjarvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leple, J.-C., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montanini, B., Napoli, C., Nelson, D.R., Nelson, D., Nieminen, K., Nilsson, O., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouze, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, C., Uberbacher, E., Unneberg, P., and Vahala, J.

Subjects
Basic biological sciences
Published
2006

30. The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)

Author

Tuskan, G. A., DiFazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., Putnam, N., Ralph, S., Rombauts, S., Salamov, A., Schein, J., Sterck, L., Aerts, A., Bhalerao, R. R., Bhalerao, R. P., Blaudez, D., Boerjan, W., Brun, A., Brunner, A., Busov, V., Campbell, M., Carlson, J., Chalot, M., Chapman, J., Chen, G.-L., Cooper, D., Coutinho, P. M., Couturier, J., Covert, S., Cronk, Q., Cunningham, R., Davis, J., Degroeve, S., Déjardin, A., dePamphilis, C., Detter, J., Dirks, B., Dubchak, I., Duplessis, S., Ehlting, J., Ellis, B., Gendler, K., Goodstein, D., Gribskov, M., Grimwood, J., Groover, A., Gunter, L., Hamberger, B., Heinze, B., Helariutta, Y., Henrissat, B., Holligan, D., Holt, R., Huang, W., Islam-Faridi, N., Jones, S., Jones-Rhoades, M., Jorgensen, R., Joshi, C., Kangasjärvi, J., Karlsson, J., Kelleher, C., Kirkpatrick, R., Kirst, M., Kohler, A., Kalluri, U., Larimer, F., Leebens-Mack, J., Leplé, J.-C., Locascio, P., Lou, Y., Lucas, S., Martin, F., Montanini, B., Napoli, C., Nelson, D. R., Nelson, C., Nieminen, K., Nilsson, O., Pereda, V., Peter, G., Philippe, R., Pilate, G., Poliakov, A., Razumovskaya, J., Richardson, P., Rinaldi, C., Ritland, K., Rouzé, P., Ryaboy, D., Schmutz, J., Schrader, J., Segerman, B., Shin, H., Siddiqui, A., Sterky, F., Terry, A., Tsai, C.-J., Uberbacher, E., Unneberg, P., Vahala, J., Wall, K., Wessler, S., Yang, G., Yin, T., Douglas, C., Marra, M., Sandberg, G., Van de Peer, Y., and Rokhsar, D.

Published
2006

40. Microtubule dynamics analysis using kymographs and variable-rate particle filters

Author

Smal, I., Grigoriev, I., Akhmanova, A., Niessen, W.J., and Meijering, E.

Subjects
Bayesian statistical decision theory -- Methods, Digital filters -- Innovations, Image segmentation -- Usage, Microscope and microscopy -- Technology application, Technology application, Business, Computers, Electronics, Electronics and electrical industries
Published
2010

48. 101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens

Author

Haridas, S., Albert, R., Binder, M., Bloem, J., LaButti, K., Salamov, A., Andreopoulos, B., Baker, S. E., Barry, K., Bills, G., Bluhm, B. H., Cannon, C., Castanera, R., Culley, D. E., Daum, C., Ezra, D., González, J. B., Henrissat, B., Kuo, A., Liang, C., Lipzen, A., Lutzoni, F., Magnuson, J., Mondo, S. J., Nolan, M., Ohm, R. A., Pangilinan, J., Park, H. J., Ramírez, L., Alfaro, M., Sun, H., Tritt, A., Yoshinaga, Y., Zwiers, L. H., Turgeon, B. G., Goodwin, S. B., Spatafora, J. W., Crous, P. W., Grigoriev, I. V., Haridas, S., Albert, R., Binder, M., Bloem, J., LaButti, K., Salamov, A., Andreopoulos, B., Baker, S. E., Barry, K., Bills, G., Bluhm, B. H., Cannon, C., Castanera, R., Culley, D. E., Daum, C., Ezra, D., González, J. B., Henrissat, B., Kuo, A., Liang, C., Lipzen, A., Lutzoni, F., Magnuson, J., Mondo, S. J., Nolan, M., Ohm, R. A., Pangilinan, J., Park, H. J., Ramírez, L., Alfaro, M., Sun, H., Tritt, A., Yoshinaga, Y., Zwiers, L. H., Turgeon, B. G., Goodwin, S. B., Spatafora, J. W., Crous, P. W., and Grigoriev, I. V.

Abstract

Dothideomycetes is the largest class of kingdom Fungi and comprises an incredible diversity of lifestyles, many of which have evolved multiple times. Plant pathogens represent a major ecological niche of the class Dothideomycetes and they are known to infect most major food crops and feedstocks for biomass and biofuel production. Studying the ecology and evolution of Dothideomycetes has significant implications for our fundamental understanding of fungal evolution, their adaptation to stress and host specificity, and practical implications with regard to the effects of climate change and on the food, feed, and livestock elements of the agro-economy. In this study, we present the first large-scale, whole-genome comparison of 101 Dothideomycetes introducing 55 newly sequenced species. The availability of whole-genome data produced a high-confidence phylogeny leading to reclassification of 25 organisms, provided a clearer picture of the relationships among the various families, and indicated that pathogenicity evolved multiple times within this class. We also identified gene family expansions and contractions across the Dothideomycetes phylogeny linked to ecological niches providing insights into genome evolution and adaptation across this group. Using machine-learning methods we classified fungi into lifestyle classes with >95 % accuracy and identified a small number of gene families that positively correlated with these distinctions. This can become a valuable tool for genome-based prediction of species lifestyle, especially for rarely seen and poorly studied species.

Published
2020

49. Concerted action of kinesins KIF5B and KIF13B promotes efficient secretory vesicle transport to microtubule plus ends

Author

Serra-Marques, A. (Andrea), Martin, M. (Maud), Katrukha, E.A. (Eugene), Grigoriev, I. (Ilya), Peeters, C.A. (Cathelijn Ae), Liu, Q. (Qingyang), Hooikaas, P.J. (Peter Jan), Yao, Y. (Yao), Solianova, V. (Veronika), Smal, I. (Ihor), Pedersen, L.B. (Lotte), Meijering, H.W. (Erik), Kapitein, L.C. (Lukas), Akhmanova, A.S. (Anna), Serra-Marques, A. (Andrea), Martin, M. (Maud), Katrukha, E.A. (Eugene), Grigoriev, I. (Ilya), Peeters, C.A. (Cathelijn Ae), Liu, Q. (Qingyang), Hooikaas, P.J. (Peter Jan), Yao, Y. (Yao), Solianova, V. (Veronika), Smal, I. (Ihor), Pedersen, L.B. (Lotte), Meijering, H.W. (Erik), Kapitein, L.C. (Lukas), and Akhmanova, A.S. (Anna)

Abstract

Intracellular transport relies on multiple kinesins, but it is poorly understood which kinesins are present on particular cargos, what their contributions are and whether they act simultaneously on the same cargo. Here, we show that Rab6-positive secretory vesicles are transported from the Golgi apparatus to the cell periphery by kinesin-1 KIF5B and kinesin-3 KIF13B, which determine the location of secretion events. KIF5B plays a dominant role, whereas KIF13B helps Rab6 vesicles to reach freshly polymerized microtubule ends, to which KIF5B binds poorly, likely because its cofactors, MAP7-family proteins, are slow in populating these ends. Sub-pixel localization demonstrated that during microtubule plus-end directed transport, both kinesins localize to the vesicle front and can be engaged on the same vesicle. When vesicles reverse direction, KIF13B relocates to the middle of the vesicle, while KIF5B shifts to the back, suggesting that KIF5B but not KIF13B undergoes a tug-of-war with a minus-end directed motor.

Published
2020
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50. 101 Dothideomycetes genomes: A test case for predicting lifestyles and emergence of pathogens

Author

Sub Molecular Microbiology, Molecular Microbiology, Haridas, S., Albert, R., Binder, M., Bloem, J., LaButti, K., Salamov, A., Andreopoulos, B., Baker, S. E., Barry, K., Bills, G., Bluhm, B. H., Cannon, C., Castanera, R., Culley, D. E., Daum, C., Ezra, D., González, J. B., Henrissat, B., Kuo, A., Liang, C., Lipzen, A., Lutzoni, F., Magnuson, J., Mondo, S. J., Nolan, M., Ohm, R. A., Pangilinan, J., Park, H. J., Ramírez, L., Alfaro, M., Sun, H., Tritt, A., Yoshinaga, Y., Zwiers, L. H., Turgeon, B. G., Goodwin, S. B., Spatafora, J. W., Crous, P. W., Grigoriev, I. V., Sub Molecular Microbiology, Molecular Microbiology, Haridas, S., Albert, R., Binder, M., Bloem, J., LaButti, K., Salamov, A., Andreopoulos, B., Baker, S. E., Barry, K., Bills, G., Bluhm, B. H., Cannon, C., Castanera, R., Culley, D. E., Daum, C., Ezra, D., González, J. B., Henrissat, B., Kuo, A., Liang, C., Lipzen, A., Lutzoni, F., Magnuson, J., Mondo, S. J., Nolan, M., Ohm, R. A., Pangilinan, J., Park, H. J., Ramírez, L., Alfaro, M., Sun, H., Tritt, A., Yoshinaga, Y., Zwiers, L. H., Turgeon, B. G., Goodwin, S. B., Spatafora, J. W., Crous, P. W., and Grigoriev, I. V.

Published
2020

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