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    Rice paddy soils are a quantitatively important carbon store according to a global synthesis

    1.Batjes, N. H. Total carbon and nitrogen in the soils of the world. Eur. J. Soil Sci. 65, 10–21 (1996).Article 
    CAS 

    Google Scholar 
    2.Lal, R. Soil carbon sequestration impacts on global climate change and food security. Science 304, 1623–1627 (2004).CAS 
    Article 

    Google Scholar 
    3.Buringh, P. in The role of terrestrial vegetation in the global carbon cycle: Measurement by remote sensing, 91–109 (Wiley, 1984).4.Hiederer, R. & Köchy, M. Global soil organic carbon estimates and the harmonized world soil database. EUR 79, 25225 (2011).
    Google Scholar 
    5.Smith, P. et al. Global change pressures on soils from land use and management. Glob. Chang. Biol. 22, 1008–1028 (2016).Article 

    Google Scholar 
    6.Schlesinger, W. H. The Role of Terrestrial Vegetation in the Global Carbon Cycle: Measurement by Remote Sensing (Wiley, 1984).7.Conant, R. T., Cerri, C. E., Osborne, B. B. & Paustian, K. Grassland management impacts on soil carbon stocks: a new synthesis. Ecol. Appl. 27, 662–668 (2017).Article 

    Google Scholar 
    8.Köchy, M., Hiederer, R. & Freibauer, A. Global distribution of soil organic carbon–Part 1: masses and frequency distributions of SOC stocks for the tropics, permafrost regions, wetlands, and the world. Soil 1, 351–365 (2015).Article 
    CAS 

    Google Scholar 
    9.Nahlik, A. M. & Fennessy, M. S. Carbon storage in US wetlands. Nat. Commun. 7, 1–9 (2016).Article 
    CAS 

    Google Scholar 
    10.Dixon, R. K. et al. Carbon pools and flux of global forest ecosystems. Science 263, 185–190 (1994).CAS 
    Article 

    Google Scholar 
    11.Atwood, T. B. et al. Global patterns in mangrove soil carbon stocks and losses. Nat. Clim. Chang. 7, 523–528 (2017).CAS 
    Article 

    Google Scholar 
    12.Maclean, J. L., Dawe, D. C., Hardy, B. & Hettel, G. P. Rice Almanac: Source book for the most important economic activity on earth, 3rd edn. (CABI Publishing, 2002).13.Kögel-Knabner, I. et al. Biogeochemistry of paddy soils. Geoderma 157, 1–14 (2010).Article 
    CAS 

    Google Scholar 
    14.Wu, J. Carbon accumulation in paddy ecosystems in subtropical China: evidence from landscape studies. Eur. J. Soil Sci. 62, 29–34 (2011).CAS 
    Article 

    Google Scholar 
    15.Carlson, K. M. et al. Greenhouse gas emissions intensity of global croplands. Nat. Clim. Chang. 7, 63–68 (2017).CAS 
    Article 

    Google Scholar 
    16.FAO (Food and Agriculture Organization of the United Nations). FAOSTAT: FAO Statistical Databases. http://faostat.fao.org/default.aspx (2018).17.Gattinger, A. et al. Enhanced top soil carbon stocks under organic farming. Proc. Natl Acad. Sci. USA 109, 18226–18231 (2012).CAS 
    Article 

    Google Scholar 
    18.Xie, Z. et al. Soil organic carbon stocks in China and changes from 1980s to 2000s. Glob. Chang. Biol. 13, 1989–2007 (2007).Article 

    Google Scholar 
    19.Qin, Z., Huang, Y. & Zhuang, Q. Soil organic carbon sequestration potential of cropland in China. Glob. Biogeochem. Cycles 27, 711–722 (2013).CAS 
    Article 

    Google Scholar 
    20.Jobbágy, E. G. & Jackson, R. B. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecol. Appl. 10, 423–436 (2000).Article 

    Google Scholar 
    21.Haefele, S. M., Nelson, A. & Hijmans, R. J. Soil quality and constraints in global rice production. Geoderma 235, 250–259 (2014).Article 
    CAS 

    Google Scholar 
    22.Pan, G., Li, L., Wu, L. & Zhang, X. Storage and sequestration potential of topsoil organic carbon in China’s paddy soils. Glob. Chang. Biol. 10, 79–92 (2004).Article 

    Google Scholar 
    23.Wei, L. et al. Comparing carbon and nitrogen stocks in paddy and upland soils: Accumulation, stabilization mechanisms, and environmental drivers. Geoderma 398, 115121 (2021).Article 

    Google Scholar 
    24.Wang, P. et al. Long-term rice cultivation stabilizes soil organic carbon and promotes soil microbial activity in a salt marsh derived soil chronosequence. Sci. Rep. 5, 15704 (2015).CAS 
    Article 

    Google Scholar 
    25.Li, Y. et al. Oxygen availability determines key regulators in soil organic carbon mineralisation in paddy soils. Soil Biol. Biochem. 153, 108106 (2021).CAS 
    Article 

    Google Scholar 
    26.Evans, C. D. et al. Acidity controls on dissolved organic carbon mobility in organic soils. Glob. Chang. Biol. 18, 3317–3331 (2012).Article 

    Google Scholar 
    27.Liu, Y. et al. Impact of prolonged rice cultivation on coupling relationship among C, Fe, and Fe-reducing bacteria over a 1000-year paddy soil chronosequence. Biol. Fertil. Soils 55, 589–602 (2019).CAS 
    Article 

    Google Scholar 
    28.Sinsabaugh, R. L. et al. Stoichiometry of soil enzyme activity at global scale. Ecol. Lett. 11, 1252–1264 (2008).Article 

    Google Scholar 
    29.Liu, Y. et al. Microbial activity promoted with organic carbon accumulation in macroaggregates of paddy soils under long-term rice cultivation. Biogeosciences 13, 6565–6586 (2016).CAS 
    Article 

    Google Scholar 
    30.Liu, Y. et al. Methanogenic abundance and changes in community structure along a rice soil chronosequence from east China. Eur. J. Soil Sci. 67, 443–455 (2016).CAS 
    Article 

    Google Scholar 
    31.Malik, A. A. et al. Land use driven change in soil pH affects microbial carbon cycling processes. Nat. Commun. 9, 1–10 (2018).CAS 
    Article 

    Google Scholar 
    32.Don, A., Schumacher, J. & Freibauer, A. Impact of tropical land‐use change on soil organic carbon stocks-a meta‐analysis. Glob. Chang. Biol. 17, 1658–1670 (2011).Article 

    Google Scholar 
    33.Piao, S. et al. The carbon balance of terrestrial ecosystems in China. Nature 458, 1009–1013 (2009).CAS 
    Article 

    Google Scholar 
    34.Davidson, E. A. & Janssens, I. A. Temperature sensitivity of soil carbon decomposition and feedbacks to climate change. Nature 440, 165–173 (2006).CAS 
    Article 

    Google Scholar 
    35.Kirk, G. The Biogeochemistry of Submerged Soils (Wiley, 2004).36.Kramer, M. G., Sanderman, J., Chadwick, O. A., Chorover, J. & Vitousek, P. M. Long‐term carbon storage through retention of dissolved aromatic acids by reactive particles in soil. Glob. Chang. Biol. 18, 2594–2605 (2012).Article 

    Google Scholar 
    37.Scharpenseel, H. W., Pfeiffer, E. M. & Becker-Heidmann, P. in Advances in Soil Science (eds. Carter, MR, Stewart, BA) (Lewis Publishers, 1996).38.Liao, Q. et al. Increase in soil organic carbon stock over the last two decades in China’s Jiangsu Province. Glob. Chang. Biol. 15, 861–875 (2009).Article 

    Google Scholar 
    39.Keiluweit, M., Wanzek, T., Kleber, M., Nico, P. & Fendorf, S. Anaerobic microsites have an unaccounted role in soil carbon stabilization. Nat. Commun. 8, 1–10 (2017).CAS 
    Article 

    Google Scholar 
    40.Ghimire, R., Lamichhane, S., Acharya, B. S., Bista, P. & Sainju, U. M. Tillage, crop residue, and nutrient management effects on soil organic carbon in rice-based cropping systems: a review. J. Integr. Agric. 16, 1–15 (2017).Article 

    Google Scholar 
    41.Maillard, É. & Angers, D. A. Animal manure application and soil organic carbon stocks: a meta‐analysis. Glob. Chang. Biol. 20, 666–679 (2014).Article 

    Google Scholar 
    42.Tian, K. et al. Effects of long-term fertilization and residue management on soil organic carbon changes in paddy soils of China: a meta-analysis. Agric. Ecosyst. Environ. 204, 40–50 (2015).CAS 
    Article 

    Google Scholar 
    43.Liu, Y. et al. Initial utilization of rhizodeposits with rice growth in paddy soils: rhizosphere and N fertilization effects. Geoderma 338, 30–39 (2019).CAS 
    Article 

    Google Scholar 
    44.Chen, J. et al. A keystone microbial enzyme for nitrogen control of soil carbon storage. Sci. Adv. 4, eaaq1689 (2018).CAS 
    Article 

    Google Scholar 
    45.Zhu, Z. et al. Rice rhizodeposits affect organic matter decomposition in paddy soil: the role of N fertilization and rice growth for enzyme activities, CO2 and CH4 emissions. Soil Biol. Biochem. 116, 369–377 (2018).CAS 
    Article 

    Google Scholar 
    46.Moorhead, D. L. & Sinsabaugh, R. L. A theoretical model of litter decay and microbial interaction. Ecol. Monogr. 76, 151–174 (2006).Article 

    Google Scholar 
    47.Li, X. et al. Nitrogen fertilization decreases the decomposition of soil organic matter and plant residues in planted soils. Soil Biol. Biochem. 112, 47–55 (2017).CAS 
    Article 

    Google Scholar 
    48.Cui, J. et al. Carbon and nitrogen recycling from microbial necromass to cope with C:N stoichiometric imbalance by priming. Soil Biol. Biochem. 142, 107720 (2020).CAS 
    Article 

    Google Scholar 
    49.Geisseler, D., Linquist, B. A. & Lazicki, P. A. Effect of fertilization on soil microorganisms in paddy rice systems—a meta-analysis. Soil Biol. Biochem. 115, 452–460 (2017).CAS 
    Article 

    Google Scholar 
    50.Sun, W. et al. Climate drives global soil carbon sequestration and crop yield changes under conservation agriculture. Glob. Chang. Biol. 26, 3325–3335 (2020).Article 

    Google Scholar 
    51.Wissing, L. et al. Management-induced organic carbon accumulation in paddy soils: the role of organo-mineral associations. Soil Tillage Res. 126, 60–71 (2013).Article 

    Google Scholar 
    52.Baker, J. M., Ochsner, T. E., Venterea, R. T. & Griffis, T. J. Tillage and soil carbon sequestration—-what do we really know? Agric. Ecosyst. Environ. 118, 1–5 (2007).CAS 
    Article 

    Google Scholar 
    53.Lal, R. Challenges and opportunities in soil organic matter research. Eur. J. Soil Sci. 60, 158–169 (2009).CAS 
    Article 

    Google Scholar 
    54.Lal, R. Soil carbon sequestration in India. Clim. Change 65, 277–296 (2004).CAS 
    Article 

    Google Scholar 
    55.Liu, Y. et al. Carbon input and allocation by rice into paddy soils: a review. Soil Biol. Biochem. 133, 97–107 (2019).CAS 
    Article 

    Google Scholar 
    56.Zhao, Y. et al. Economics-and policy-driven organic carbon input enhancement dominates soil organic carbon accumulation in Chinese croplands. Proc. Natl Acad. Sci. USA 115, 4045–4050 (2018).CAS 
    Article 

    Google Scholar 
    57.Wei, X., Zhu, Z., Wei, L., Wu, J. & Ge, T. Biogeochemical cycles of key elements in the paddy-rice rhizosphere: microbial mechanisms and coupling processes. Rhizosphere 10, 100145 (2019).Article 

    Google Scholar 
    58.Alexandratos, N. & Bruinsma, J. World agriculture towards 2030/2050: the 2012 revision. https://doi.org/10.22004/ag.econ.288998. (2012).59.Rui, W. & Zhang, W. Effect size and duration of recommended management practices on carbon sequestration in paddy field in Yangtze Delta Plain of China: a meta-analysis. Agric. Ecosyst. Environ. 135, 199–205 (2010).CAS 
    Article 

    Google Scholar 
    60.Song, K. et al. Wetland degradation: its driving forces and environmental impacts in the Sanjiang Plain, China. Environ. Manage. 54, 255–271 (2014).Article 

    Google Scholar 
    61.Dong, J. et al. Northward expansion of paddy rice in northeastern Asia during 2000–2014. Geophys. Res. Lett. 43, 3754–3761 (2016).CAS 
    Article 

    Google Scholar 
    62.Chaturvedi, V. et al. Climate mitigation policy implications for global irrigation water demand. Mitig. Adapt. Strat. Glob. Chang. 20, 389–407 (2015).Article 

    Google Scholar 
    63.Gathorne-Hardy, A. A life cycle assessment (LCA) of greenhouse gas emissions from SRI and flooded rice production in SE India. Taiwan Water Conserv. J. 61, 111–125 (2013).
    Google Scholar 
    64.Linquist, B., Van Groenigen, K. J., Adviento‐Borbe, M. A., Pittelkow, C. & Van Kessel, C. An agronomic assessment of greenhouse gas emissions from major cereal crops. Glob. Chang. Biol. 18, 194–209 (2012).Article 

    Google Scholar 
    65.IPCC. in Contribution of working group II to the fifth assessment report of the Intergovernmental Panel on Climate Change. (eds. Field, C. B. et al) (Cambridge University Press, 2014).66.Xie, Z. et al. CO2 mitigation potential in farmland of China by altering current organic matter amendment pattern. Sci. China Earth Sci. 53, 1351–1357 (2010).CAS 
    Article 

    Google Scholar 
    67.Yan, X. et al. Carbon sequestration efficiency in paddy soil and upland soil under long-term fertilization in southern China. Soil Tillage Res. 130, 42–51 (2013).Article 

    Google Scholar 
    68.Shang, Q. et al. Net annual global warming potential and greenhouse gas intensity in Chinese double rice‐cropping systems: a 3‐year field measurement in long‐term fertilizer experiments. Glob. Chang. Biol. 17, 2196–2210 (2011).Article 

    Google Scholar 
    69.Ma, Y. et al. Net global warming potential and greenhouse gas intensity of annual rice–wheat rotations with integrated soil–crop system management. Agric. Ecosyst. Environ. 164, 209–219 (2013).Article 

    Google Scholar 
    70.Xiong, Z. et al. Differences in net global warming potential and greenhouse gas intensity between major rice-based cropping systems in China. Sci. Rep. 5, 1–9 (2015).CAS 

    Google Scholar 
    71.Jiang, Y. et al. Acclimation of methane emissions from rice paddy fields to straw addition. Sci. Adv. 5, eaau9038 (2019).Article 
    CAS 

    Google Scholar 
    72.Liu, C., Lu, M., Cui, J., Li, B. & Fang, C. Effects of straw carbon input on carbon dynamics in agricultural soils: a meta‐analysis. Glob. Chang. Biol. 20, 1366–1381 (2014).Article 

    Google Scholar 
    73.Shakoor, A. et al. A global meta-analysis of greenhouse gases emission and crop yield under no-tillage as compared to conventional tillage. Sci. Total Environ. 750, 142299 (2021).CAS 
    Article 

    Google Scholar 
    74.Zhao, X. et al. Methane and nitrous oxide emissions under no‐till farming in China: a meta‐analysis. Glob. Chang. Biol. 22, 1372–1384 (2016).Article 

    Google Scholar 
    75.Kim, S. Y., Gutierrez, J. & Kim, P. J. Unexpected stimulation of CH4 emissions under continuous no-tillage system in mono-rice paddy soils during cultivation. Geoderma 267, 34–40 (2016).CAS 
    Article 

    Google Scholar 
    76.Ball, B. C., Scott, A. & Parker, J. P. Field N2O, CO2 and CH4 fluxes in relation to tillage, compaction and soil quality in Scotland. Soil Tillage Res. 53, 29–39 (1999).Article 

    Google Scholar 
    77.Linquist, B. A., Adviento-Borbe, M. A., Pittelkow, C. M., van Kessel, C. & van Groenigen, K. J. Fertilizer management practices and greenhouse gas emissions from rice systems: a quantitative review and analysis. Field Crop. Res. 135, 10–21 (2012).Article 

    Google Scholar 
    78.Schlesinger, W. H. Carbon sequestration in soils: some cautions amidst optimism. Agric. Ecosyst. Environ. 82, 121–127 (2000).CAS 
    Article 

    Google Scholar 
    79.Choudhury, A. T. M. A. & Kennedy, I. R. Nitrogen fertilizer losses from rice soils and control of environmental pollution problems. Commun. Soil Sci. Plan. 36, 1625–1639 (2005).CAS 
    Article 

    Google Scholar 
    80.Jiang, Y. et al. Water management to mitigate the global warming potential of rice systems: a global meta-analysis. Field Crop. Res. 234, 47–54 (2019).Article 

    Google Scholar 
    81.Suryavanshi, P., Singh, Y. V., Prasanna, R., Bhatia, A. & Shivay, Y. S. Pattern of methane emission and water productivity under different methods of rice crop establishment. Paddy Water Environ. 11, 321–329 (2013).Article 

    Google Scholar 
    82.Yan, X., Akiyama, H., Yagi, K. & Akimoto, H. Global estimations of the inventory and mitigation potential of methane emissions from rice cultivation conducted using the 2006 Intergovernmental Panel on Climate Change Guidelines. Glob. Biogeochem. Cycles https://doi.org/10.1029/2008GB003299 (2009).83.Jiang, Y. et al. Higher yields and lower methane emissions with new rice cultivars. Glob. Chang. Biol. 23, 4728–4738 (2017).Article 

    Google Scholar 
    84.Li, C. et al. Modeling greenhouse gas emissions from rice-based production systems: sensitivity and upscaling. Glob. Biogeochem. Cycles https://doi.org/10.1029/2003GB002045 (2004).85.Yin, S. et al. Carbon sequestration and emissions mitigation in paddy fields based on the DNDC model: a review. Artif. Intell. Agric. 4, 140–149 (2020).
    Google Scholar 
    86.FAO, IIASA, ISRIC, ISSCAS, and JRC: Harmonized World Soil Database (version 1.2), Tech. Rep., FAO, Rome, Italy and IIASA, Laxenburg, Austria (2012).87.Allison, L. in Organic carbon. Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties, (ed. A.g. Norman). (American Society of Agronomy, 1965).88.Fang, C. & Moncrieff, J. B. The variation of soil microbial respiration with depth in relation to soil carbon composition. Plant Soil 268, 243–253 (2005).CAS 
    Article 

    Google Scholar 
    89.Yan, X., Cai, Z., Wang, S. & Smith, P. Direct measurement of soil organic carbon content change in the croplands of China. Glob. Chang. Biol. 17, 1487–1496 (2011).Article 

    Google Scholar 
    90.Rosenberg, M. S., Adams, D. C. & Gurevitch, J. MetaWin 2.0: statistical software for meta-analysis (Sinauer, 2000).91.Yue, Q. et al. Deriving emission factors and estimating direct nitrous oxide emissions for crop cultivation in China. Environ. Sci. Technol. 53, 10246–10257 (2019).CAS 
    Article 

    Google Scholar 
    92.Hedges, L. V., Gurevitch, J. & Curtis, P. S. The meta‐analysis of response ratios in experimental ecology. Ecology 80, 1150–1156 (1999).Article 

    Google Scholar 
    93.Adams, D. C., Gurevitch, J. & Rosenberg, M. S. Resampling tests for meta‐analysis of ecological data. Ecology 78, 1277–1283 (1997).Article 

    Google Scholar 
    94.Van Groenigen, K. J., Osenberg, C. W. & Hungate, B. A. Increased soil emissions of potent greenhouse gases under increased atmospheric CO2. Nature 475, 214–216 (2011).Article 
    CAS 

    Google Scholar  More

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    An insight of anopheline larvicidal mechanism of Trichoderma asperellum (TaspSKGN2)

    1.Ghosh, S. K., Podder, D., Panja, S., & Mukherjee, S. In target areas where human mosquito-borne diseases are diagnosed, the inclusion of the pre-adult mosquito aquatic niches parameters will improve the integrated mosquito control program. PLos Neg. Trop. Dis. 14(8), e0008605 (2020).Article 

    Google Scholar 
    2.Becker, B. N. et al. Mosquitoes and Their Control 499 (Springer, 2010).Book 

    Google Scholar 
    3.Hyde, K. D. et al. The amazing potential of fungi: 50 ways we can exploit fungi industrially. Fungal Divers. 97, 1–136 (2019).Article 

    Google Scholar 
    4.Clark, T. B., Kellen, W. R., Fukuda, T. & Lindegren, J. E. Field and laboratory studies on the pathogenicity of the fungus Beauveria bassiana to three genera of mosquitoes. J. Invertebr. Pathol. 11(1), 1–7 (1968).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    5.Scholte, E. J., Knols, B. G. & Takken, W. Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. J. Invertebr. Pathol. 91(1), 43–49 (2006).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    6.Bukhari, T., Takken, W. & Koenraadt, C. J. Development of Metarhizium anisopliae and Beauveria bassiana formulations for control of malaria mosquito larvae. Parasit. Vectors 4(1), 23 (2011).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.Mukherjee, A., Debnath, P., Ghosh, S. K. & Medda, P. K. Biological control of papaya aphid (Aphis gossypii Glover) using entomopathogenic fungi. Vegetos 33, 1–10 (2020).Article 

    Google Scholar 
    8.Fernández-Grandon, G. M., Harte, S. J., Ewany, J., Bray, D. & Stevenson, P. C. Additive effect of botanical insecticide and entomopathogenic fungi on pest mortality and the behavioral response of its natural enemy. Plants 9, 173 (2020).PubMed Central 
    Article 
    CAS 

    Google Scholar 
    9.Sobczak, J. F. et al. Manipulation of wasp (Hymenoptera: Vespidae) behavior by the entomopathogenic fungus Ophiocordyceps humbertii in the Atlantic forest in Ceará, Brazil. Entomol. News 129, 98–104 (2020).Article 

    Google Scholar 
    10.Ghosh, S. K. & Pal, S. Entomopathogenic potential of Trichoderma longibrachiatum and its comparative evaluation with malathion against the insect pest Leucinodes orbonalis. Environ. Monit. Assess. 188(1), 37 (2016).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar 
    11.Podder, D. & Ghosh, S. K. A new application of Trichoderma asperellum as an anopheline larvicide for eco friendly management in medical science. Sci. Reps. 9(1), 1108 (2019).ADS 
    Article 
    CAS 

    Google Scholar 
    12.Jones, E. B. G. Fungal adhesion. Mycol. Res. 98(9), 961–981 (1994).Article 

    Google Scholar 
    13.Shah, P. A. & Pell, J. K. Entomopathogenic fungi as biological control agents. Appl. Microbiol. Biotechnol. 61, 413–423 (2003).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    14.Rudall, K. M. The chitin/protein complexes of insect cuticles. Adv. Insect Physiol. 1, 257–313 (1963).ADS 
    CAS 
    Article 

    Google Scholar 
    15.Shah, F. A., Wang, C. S. & Butt, T. M. Nutrition influences growth and virulence of the insect-pathogenic fungus Metarhizium anisopliae. FEMS Microbiol. Lett. 251(2), 259–266 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    16.Jackson, M. A., Dunlap, C. A. & Jaronski, S. T. Ecological considerations in producing and formulating fungal entomopathogens for use in insect biocontrol. Biocontrol 55(1), 129–145 (2010).Article 

    Google Scholar 
    17.Vega, F.E.; Meyling, N., Luangsa-ard, J.& Blackwell, M. Fungal entomopathogens. In: edit Vega, F. and Kaya, H. A. Insect pathology, 2nd edn , San Diego, CA, Academic Press, pp 171–220 (2012).18.Gaugler, R. Entomopathogenic nematodes in biological control. CRC press (2018).19.McKinnon, A. C. et al. Detection of the entomopathogenic fungus Beauveria bassiana in the rhizosphere of wound-stressed zea mays plants. Front. Microbiol. 9, 1161 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    20.Zimmermann, G. Review on safety of the entomopathogenic fungus Metarhizium anisopliae. Biocontrol Sci. Technol. 17(9), 879–920 (2007).Article 

    Google Scholar 
    21.Hamer, J. E., Howard, R. J., Chumley, F. G. & Valent, B. A mechanism for surface attachment in spores of a plant pathogenic fungus. Science 239(4837), 288–290 (1988).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    22.Dhawan, M. & Joshi, N. (Enzymatic comparison and mortality of Beauveria bassiana against cabbage caterpillar Pieris brassicae LINN. Braz. J. Microbiol. 48(3), 522–529 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    23.Mora, M. A. E., Castilho, A. M. C. & Fraga, M. E. Classification and infection mechanism of entomopathogenic fungi. Arq. Inst. Biol. 84, 0552015 (2017).
    Google Scholar 
    24.Li, J., Tracy, J. W. & Christensen, B. M. Phenol oxidase activity in hemolymph compartments of Aedes aegypti during melanotic encapsulation reactions against microfilariae. Dev. Comp. Immunol. 16(1), 41–48 (1992).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    25.Hillyer, J. F. & Strand, M. R. Mosquito hemocyte-mediated immune responses. Curr. Opin. Insect Sci. 3, 14–21 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Nanda, K. P. Chronic lead (Pb) exposure results in diminished hemocyte count and increased susceptibility to bacterial infection in Drosophila melanogaster. Chemosphere 236, 124349 (2019).ADS 
    CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    27.Ghosh, S. K., Chatterjee, T., Chakravarty, A. & Basak, A. K. Sodium and potassium nitrite-induced developmental genotoxicity in Drosophila melanogaster—effects in larval immune and brain stem cells. Interdiscip. Toxicol. 13(4), 101–105 (2020).
    Google Scholar 
    28.Chatterjee, T., Ghosh, S. K., Paik, S., Chakravarty, A. & Basak, A. K. Benzoic acid treated Drosophila melanogaster the genetic disruption of larval brain stem cells and non-neural cells during metamorphosis. Toxicol. Environ. Health Sci. https://doi.org/10.1007/s13530-021-00082-w (2021).Article 

    Google Scholar 
    29.Campos, R. A. Boophilus microplus infection by Beauveria amorpha and Beauveria bassiana: SEM analysis and regulation of subtilisin-like proteases and chitinases. Curr. Microbiol. 50(5), 257–261 (2005).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    30.McFarlane, H. E., Gendre, D. & Western, T. L. Seed coat ruthenium red staining assay. Bio-Protoc. 4, 1096 (2014).Article 

    Google Scholar 
    31.Bhosale, R. R., Osmani, R. A. M. & Moin, A. Natural gums and mucilages: A review on multifaceted excipients in pharmaceutical science and research. Int. J. Res. Phytochem. Pharmacol 6(4), 901–912 (2014).
    Google Scholar 
    32.Shah, F. A., Allen, N., Wright, C. J. & Butt, T. M. Repeated in vitro subculturing alters spore surface properties and virulence of Metarhizium anisopliae. FEMS Microbiol. Lett. 276(1), 60–66 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    33.Hsu, S. C. & Lockwood, J. L. Powdered chitin agar as a selective medium for enumeration of actinomycetes in water and soil. Appl. Environ. Microbiol. 29(3), 422–426 (1975).CAS 
    Article 

    Google Scholar 
    34.Parida, D., Jena, S. K. & Rath, C. C. Enzyme activities of bacterial isolates from iron mine areas of Barbil, Keonjhar district, Odisha, India. Int. J. Pure Appl. Biosci. 2(3), 265–271 (2014).
    Google Scholar 
    35.Kasana, R. C., Salwan, R., Dhar, H., Dutt, S. & Gulati, A. A rapid and easy method for the detection of microbial cellulases on agar plates using Gram’s iodine. Curr. Microbiol. 57(5), 503–507 (2008).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    36.Medina, P. & Baresi, L. Rapid identification of gelatin and casein hydrolysis using TCA. J. Microbiol. Methods 69(2), 391–393 (2007).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    37.Al-Nahdi, H. S. Isolation and screening of extracellular proteases produced by new isolated Bacillus sp. J. Appl. Pharm. Sci. 2(9), 71–74 (2012).CAS 

    Google Scholar 
    38.Murthy, N. K. & Bleakley, B. H. Simplified method of preparing colloidal chitin used for screening of chitinase-producing microorganisms. Int. J. Microbiol. 10(2), 1937–8289 (2012).
    Google Scholar 
    39.Park, S. H., Lee, J. H. & Lee, H. K. Purification and characterization of chitinase from a marine bacterium, Vibrio sp. 98CJ11027. J. Microbiol 38, 224–229 (2000).CAS 

    Google Scholar 
    40.Roberts, W. K. & Selitrennikoff, C. P. Plant and bacterial chitinases differ in antifungal activity. Microbiology 134(1), 169–176 (1986).Article 

    Google Scholar 
    41.Tsuchida, O. et al. An alkaline proteinase of an alkalophilic Bacillus sp. Curr. Microbiol. 14(1), 7–12 (1986).CAS 
    Article 

    Google Scholar 
    42.Crowell, A. M., Wall, M. J. & Doucette, A. A Maximizing recovery of water-soluble proteins through acetone precipitation. Anal. Chim. Acta. 796, 48–54 (2013).CAS 
    PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    43.He, F. BCA (Bicinchoninic Acid) protein assay. Bio Protocol 1(5), 44 (2011).Article 

    Google Scholar 
    44.Sierra, L.M., Carmona, E.R., Aguado, L. & Marcos, R. The comet assay in Drosophila: neuroblast and hemocyte cells. In Genotoxicity and DNA Repair. Methods in Pharmacology and Toxicology. Humana Press, New York, NY. 269–82 (2014).45.Xu, T. et al. (2012) HMGB in mollusk Crassostrea ariakensis Gould: structure, pro-inflammatory cytokine function characterization and anti-infection role of its antibody. PLoS ONE 7(11), e50789 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Basak, A. K., Chatterjee, T., Chakravarty, A. & Ghosh, S. K. Silver nanoparticle-induced developmental inhibition of Drosophila melanogaster accompanies disruption of genetic material of larval neural stem cells and non-neuronal cells. Environ. Monit. Assess. 191(8), 497 (2019).PubMed 
    Article 
    CAS 
    PubMed Central 

    Google Scholar  More

  • in

    Harnessing the power of host–microbe symbioses to address grand challenges

    1.McFall-Ngai, M. et al. Animals in a bacterial world: a new imperative for the life sciences. Proc. Natl Acad. Sci. 110, 3229–3236 (2013).CAS 
    Article 

    Google Scholar 
    2.Pita, L., Rix, L., Slaby, B. M., Franke, A. & Hentschel, U. The sponge holobiont in a changing ocean: from microbes to ecosystems. Microbiome 6, 46 (2018).CAS 
    Article 

    Google Scholar 
    3.Caruso, R., Lo, B. C. & Núñez, G. Host–microbiota interactions in inflammatory bowel disease. Nat. Rev. Immunol. 20, 411–426 (2020).CAS 
    Article 

    Google Scholar 
    4.Hughes, T. P. et al. Spatial and temporal patterns of mass bleaching of corals in the Anthropocene. Science 359, 80–83 (2018).CAS 
    Article 

    Google Scholar 
    5.Scheele, B. C. et al. Amphibian fungal panzootic causes catastrophic and ongoing loss of biodiversity. Science 363, 1459–1463 (2019).CAS 
    Article 

    Google Scholar 
    6.Bell, J. J., Bennett, H. M., Rovellini, A. & Webster, N. S. Sponges to be winners under near-future climate scenarios. BioScience 68, 955–968 (2018).Article 

    Google Scholar 
    7.Bosch, T. C. G., Guillemin, K. & McFall-Ngai, M. Evolutionary “experiments” in symbiosis: the study of model animals provides insights into the mechanisms underlying the diversity of host–microbe interactions. Bioessays 41, e1800256 (2019).8.Nyholm, S. V. & McFall-Ngai, M. J. A lasting symbiosis: how the Hawaiian bobtail squid finds and keeps its bioluminescent bacterial partner. Nat. Rev. Microbiol. https://doi.org/10.1038/s41579-021-00567-y (2021).Article 
    PubMed 

    Google Scholar 
    9.Visick, K. L., Stabb, E. V. & Ruby, E. G. A lasting symbiosis: how Vibrio fischeri finds a squid partner and persists within its natural host. Nat. Rev. Microbiol. https://doi.org/10.1038/s41579-021-00557-0 (2021).Article 
    PubMed 

    Google Scholar 
    10.Peixoto, R. S. et al. Coral probiotics: premise, promise, prospects. Annu. Rev. Anim. Biosci. 9, 265–288 (2021).Article 

    Google Scholar  More

  • in

    Gene drives gaining speed

    1.Serebrovsky, A. S. On the possibility of a new method for the control of insect pests. Zool. Zh. 19, 618–630 (1940).
    Google Scholar 
    2.Curtis, C. F. Possible use of translocations to fix desirable genes in insect pest populations. Nature 218, 368–369 (1968). This paper is one of the first to describe how reciprocal chromosomal translocations could be used to drive a favoured linked trait in a threshold-dependent fashion.CAS 
    PubMed 
    Article 

    Google Scholar 
    3.Dawkins, R. The Selfish Gene Vol. 345 (Oxford University Press, 1976).4.Bastide, H. et al. Rapid rise and fall of selfish sex-ratio X chromosomes in Drosophila simulans: spatiotemporal analysis of phenotypic and molecular data. Mol. Biol. Evol. 28, 2461–2470 (2011).CAS 
    PubMed 
    Article 

    Google Scholar 
    5.Corbett-Detig, R., Medina, P., Frerot, H., Blassiau, C. & Castric, V. Bulk pollen sequencing reveals rapid evolution of segregation distortion in the male germline of Arabidopsis hybrids. Evol. Lett. 3, 93–103 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    6.Kingan, S. B., Garrigan, D. & Hartl, D. L. Recurrent selection on the Winters sex-ratio genes in Drosophila simulans. Genetics 184, 253–265 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    7.McLaughlin, R. N. Jr. & Malik, H. S. Genetic conflicts: the usual suspects and beyond. J. Exp. Biol. 220, 6–17 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    8.Presgraves, D. C., Gerard, P. R., Cherukuri, A. & Lyttle, T. W. Large-scale selective sweep among segregation distorter chromosomes in African populations of Drosophila melanogaster. PLoS Genet. 5, e1000463 (2009).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    9.Seymour, D. K., Chae, E., Arioz, B. I., Koenig, D. & Weigel, D. Transmission ratio distortion is frequent in Arabidopsis thaliana controlled crosses. Heredity 122, 294–304 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    10.Courret, C., Chang, C. H., Wei, K. H., Montchamp-Moreau, C. & Larracuente, A. M. Meiotic drive mechanisms: lessons from Drosophila. Proc. Biol. Sci. 286, 20191430 (2019).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    11.Kusano, A., Staber, C., Chan, H. Y. & Ganetzky, B. Closing the (Ran)GAP on segregation distortion in Drosophila. Bioessays 25, 108–115 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    12.Merel, V., Boulesteix, M., Fablet, M. & Vieira, C. Transposable elements in Drosophila. Mob. DNA 11, 23 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    13.Boulesteix, M. & Biemont, C. Transposable elements in mosquitoes. Cytogenet. Genome Res. 110, 500–509 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    14.Lee, Y. C. & Langley, C. H. Transposable elements in natural populations of Drosophila melanogaster. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365, 1219–1228 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    15.Kelleher, E. S. Reexamining the P-element invasion of Drosophila melanogaster through the lens of piRNA silencing. Genetics 203, 1513–1531 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    16.Majumdar, S. & Rio, D. C. P transposable elements in drosophila and other eukaryotic organisms. Microbiol. Spectr. 3, MDNA3–0004-2014 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    17.Burns, K. H. & Boeke, J. D. Human transposon tectonics. Cell 149, 740–752 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    18.Doring, H. P., Tillmann, E. & Starlinger, P. DNA sequence of the maize transposable element Dissociation. Nature 307, 127–130 (1984).CAS 
    PubMed 
    Article 

    Google Scholar 
    19.Wallau, G. L., Capy, P., Loreto, E. & Hua-Van, A. Genomic landscape and evolutionary dynamics of mariner transposable elements within the Drosophila genus. BMC Genomics 15, 727 (2014).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    20.Hawkins, J. S., Hu, G., Rapp, R. A., Grafenberg, J. L. & Wendel, J. F. Phylogenetic determination of the pace of transposable element proliferation in plants: copia and LINE-like elements in Gossypium. Genome 51, 11–18 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    21.Biemont, C., Vieira, C., Borie, N. & Lepetit, D. Transposable elements and genome evolution: the case of Drosophila simulans. Genetica 107, 113–120 (1999).CAS 
    PubMed 
    Article 

    Google Scholar 
    22.Buchman, A. B., Ivy, T., Marshall, J. M., Akbari, O. S. & Hay, B. A. Engineered reciprocal chromosome translocations drive high threshold, reversible population replacement in drosophila. ACS Synth. Biol. 7, 1359–1370 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    23.Akbari, O. S. et al. Novel synthetic Medea selfish genetic elements drive population replacement in Drosophila; a theoretical exploration of Medea-dependent population suppression. ACS Synth. Biol. 3, 915–928 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    24.Buchman, A., Marshall, J. M., Ostrovski, D., Yang, T. & Akbari, O. S. Synthetically engineered Medea gene drive system in the worldwide crop pest Drosophila suzukii. Proc. Natl Acad. Sci. USA 115, 4725–4730 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    25.Champer, J., Zhao, J., Champer, S. E., Liu, J. & Messer, P. W. Population dynamics of underdominance gene drive systems in continuous space. ACS Synth. Biol. 9, 779–792 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    26.Chen, C. C. et al. EXO1 suppresses double-strand break induced homologous recombination between diverged sequences in mammalian cells. DNA Repair. 57, 98–106 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    27.Leftwich, P. T. et al. Recent advances in threshold-dependent gene drives for mosquitoes. Biochem. Soc. Trans. 46, 1203–1212 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    28.Raban, R. R., Marshall, J. M. & Akbari, O. S. Progress towards engineering gene drives for population control. J. Exp. Biol. 223 (Suppl. 1), jeb208181 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    29.Ward, C. M. et al. Medea selfish genetic elements as tools for altering traits of wild populations: a theoretical analysis. Evolution 65, 1149–1162 (2011).PubMed 
    Article 

    Google Scholar 
    30.Oberhofer, G., Ivy, T. & Hay, B. A. Gene drive and resilience through renewal with next generation Cleave and Rescue selfish genetic elements. Proc. Natl Acad. Sci. USA 117, 9013–9021 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    31.Oberhofer, G., Ivy, T. & Hay, B. A. Cleave and Rescue, a novel selfish genetic element and general strategy for gene drive. Proc. Natl Acad. Sci. USA 116, 6250–6259 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    32.Champer, J. et al. A toxin-antidote CRISPR gene drive system for regional population modification. Nat. Commun. 11, 1082 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Yen, P. S. & Failloux, A. B. A review: Wolbachia-based population replacement for mosquito control shares common points with genetically modified control approaches. Pathogens 9, 404 (2020).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    34.O’Neill, S. L. The use of wolbachia by the world mosquito program to interrupt transmission of aedes aegypti transmitted viruses. Adv. Exp. Med. Biol. 1062, 355–360 (2018).PubMed 
    Article 
    CAS 

    Google Scholar 
    35.Niang, E. H. A., Bassene, H., Fenollar, F. & Mediannikov, O. Biological control of mosquito-borne diseases: the potential of wolbachia-based interventions in an IVM framework. J. Trop. Med. 2018, 1470459 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    36.Chevalier, B. S. & Stoddard, B. L. Homing endonucleases: structural and functional insight into the catalysts of intron/intein mobility. Nucleic Acids Res. 29, 3757–3774 (2001).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    37.Macreadie, I. G., Scott, R. M., Zinn, A. R. & Butow, R. A. Transposition of an intron in yeast mitochondria requires a protein encoded by that intron. Cell 41, 395–402 (1985).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Rong, Y. S. & Golic, K. G. The homologous chromosome is an effective template for the repair of mitotic DNA double-strand breaks in Drosophila. Genetics 165, 1831–1842 (2003).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    39.Chan, Y. S., Huen, D. S., Glauert, R., Whiteway, E. & Russell, S. Optimising homing endonuclease gene drive performance in a semi-refractory species: the Drosophila melanogaster experience. PLoS ONE 8, e54130 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    40.Windbichler, N. et al. A synthetic homing endonuclease-based gene drive system in the human malaria mosquito. Nature 473, 212–215 (2011). This study is the first demonstration of nuclease-mediated gene drive in mosquitoes based on the homing endonuclease gene I-SceI.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    41.Carroll, D. Genome engineering with targetable nucleases. Annu. Rev. Biochem. 83, 409–439 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    42.Barrangou, R. et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 315, 1709–1712 (2007).CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Jinek, M. et al. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816–821 (2012). This foundational study developed the most widely used dual synthetic CRISPR system consisting of Cas9 endonuclease and gRNA components.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    44.Doudna, J. A., Sternberg, S. H. A Crack in Creation: Gene Editing and the Unthinkable Power to Control Evolution 281 (Houghton Mifflin Harcourt, 2017).45.Gantz, V. M. & Bier, E. The mutagenic chain reaction: a method for converting heterozygous to homozygous mutations. Science 348, 442–444 (2015). This study reported the first CRISPR-based gene drive in a metazoan organism (D. melanogaster) with a specialized germline.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    46.Gantz, V. M. et al. Highly efficient Cas9-mediated gene drive for population modification of the malaria vector mosquito Anopheles stephensi. Proc. Natl Acad. Sci. USA 112, E6736–E6743 (2015). This study describes the first efficient CRISPR-based gene drive system in mosquitoes, which carried a dual anti-malarial effector cassette.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    47.Hammond, A. et al. A CRISPR-Cas9 gene drive system targeting female reproduction in the malaria mosquito vector Anopheles gambiae. Nat. Biotechnol. 34, 78–83 (2016). This study describes the first efficient CRISPR-based suppression gene drive system in mosquitoes.CAS 
    PubMed 
    Article 

    Google Scholar 
    48.Kyrou, K. et al. A CRISPR-Cas9 gene drive targeting doublesex causes complete population suppression in caged Anopheles gambiae mosquitoes. Nat. Biotechnol. 36, 1062–1066 (2018). This study describes a highly efficient suppression gene drive system in mosquitoes targeting an invariant genome target site in the doublesex locus.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    49.Li, M. et al. Development of a confinable gene drive system in the human disease vector Aedes aegypti. eLife 9, e51701 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Grunwald, H. A. et al. Super-Mendelian inheritance mediated by CRISPR-Cas9 in the female mouse germline. Nature 566, 105–109 (2019). This study provided the first proof-of-principle gene drive system in mammals, which selectively sustained drive via the female germline.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.DiCarlo, J. E., Chavez, A., Dietz, S. L., Esvelt, K. M. & Church, G. M. Safeguarding CRISPR-Cas9 gene drives in yeast. Nat. Biotechnol. 33, 1250–1255 (2015). This study demonstrated CRISPR-based gene conversion in diploid yeast, which could then be transmitted meiotically.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    52.Valderrama, J. A., Kulkarni, S. S., Nizet, V. & Bier, E. A bacterial gene-drive system efficiently edits and inactivates a high copy number antibiotic resistance locus. Nat. Commun. 10, 5726 (2019). This study generalizes the concept of gene drive to bacteria, where it is applied to efficiently reduce the frequency of antibiotic reistance.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    53.Esvelt, K. M., Smidler, A. L., Catteruccia, F. & Church, G. M. Concerning RNA-guided gene drives for the alteration of wild populations. eLife 3, e03401 (2014).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    54.Adolfi, A. et al. Efficient population modification gene-drive rescue system in the malaria mosquito Anopheles stephensi. Nat. Commun. 11, 5553 (2020). This study reports on the first recoded gene drive in mosquitoes that drove efficiently through both males and females based on the process of lethal/sterile mosaicism.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    55.Champer, J. et al. A CRISPR homing gene drive targeting a haplolethal gene removes resistance alleles and successfully spreads through a cage population. Proc. Natl Acad. Sci. USA 117, 24377–24383 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    56.Kandul, N. P., Liu, J., Bennett, J. B., Marshall, J. M. & Akbari, O. S. A confinable home-and-rescue gene drive for population modification. eLife 10, e65939 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    57.Terradas, G. et al. Inherently confinable split-drive systems in Drosophila. Nat. Commun. 12, 1480 (2021). This study further develops the strategy of inserting a recoded gene drive in genes essential for viability or reproduction in the context of split drive systems.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    58.Xu, X. S., Gantz, V. M., Siomava, N. & Bier, E. CRISPR/Cas9 and active genetics-based trans-species replacement of the endogenous Drosophila kni-L2 CRM reveals unexpected complexity. eLife 6, e30281 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    59.Lopez Del Amo, V. et al. A transcomplementing gene drive provides a flexible platform for laboratory investigation and potential field deployment. Nat. Commun. 11, 352 (2020). This study reports on the reconstitution of a full gene drive from split constituent parts.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    60.Guichard, A. et al. Efficient allelic-drive in Drosophila. Nat. Commun. 10, 1640 (2019). The study develops two allelic drive systems, copy-cutting and copy-grafting, to propagate favoured alleles of an essential gene.PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    61.Kandul, N. P. et al. Assessment of a split homing based gene drive for efficient knockout of multiple genes. G3 10, 827–837 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    62.Xu, X.-R. S. et al. Active-genetic neutralizing elements for halting or deleting gene-drives. Mol. Cell 80, 246–262 (2020). This study reports on two drive-neutralizing systems that either inactivate (e-CHACR) or delete and replace (ERACR) a gene drive.CAS 
    PubMed 
    Article 

    Google Scholar 
    63.Burt, A. Site-specific selfish genes as tools for the control and genetic engineering of natural populations. Proc. Biol. Sci. 270, 921–928 (2003). This seminal modelling study provides the theoretical underpinnings for the modern gene-drive field.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    64.North, A. R., Burt, A. & Godfray, H. C. J. Modelling the potential of genetic control of malaria mosquitoes at national scale. BMC Biol. 17, 26 (2019). This study provides a comprehensive analysis of the perfomance of suppressive gene drives following iterative releases across various topographies.PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    65.North, A. R., Burt, A. & Godfray, H. C. J. Modelling the suppression of a malaria vector using a CRISPR-Cas9 gene drive to reduce female fertility. BMC Biol. 18, 98 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    66.Collins, C. M., Bonds, J. A. S., Quinlan, M. M. & Mumford, J. D. Effects of the removal or reduction in density of the malaria mosquito, Anopheles gambiae s.l., on interacting predators and competitors in local ecosystems. Med. Vet. Entomol. 33, 1–15 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    67.James, A. A. Gene drive systems in mosquitoes: rules of the road. Trends Parasitol. 21, 64–67 (2005).CAS 
    PubMed 
    Article 

    Google Scholar 
    68.Gantz, V. M. & Bier, E. The dawn of active genetics. Bioessays 38, 50–63 (2016).PubMed 
    Article 

    Google Scholar 
    69.Macias, V. M. & James, A. A. in Genetic Control of Malaria and Dengue (ed. Adelman, Z. N.) 423–444 (Elsevier Academic Press, 2015).70.Eckhoff, P. A., Wenger, E. A., Godfray, H. C. & Burt, A. Impact of mosquito gene drive on malaria elimination in a computational model with explicit spatial and temporal dynamics. Proc. Natl Acad. Sci. USA 114, E255–E264 (2017). This study provides a detailed analysis of drive parameters relevant to both suppression-based and modification-based drives and is the first to model a drive in the context of a two-dimensional environment.CAS 
    PubMed 
    Article 

    Google Scholar 
    71.Hammond, A. M. et al. The creation and selection of mutations resistant to a gene drive over multiple generations in the malaria mosquito. PLoS Genet. 13, e1007039 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    72.Joyce, E. F., Paul, A., Chen, K. E., Tanneti, N. & McKim, K. S. Multiple barriers to nonhomologous DNA end joining during meiosis in Drosophila. Genetics 191, 739–746 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    73.Bozas, A., Beumer, K. J., Trautman, J. K. & Carroll, D. Genetic analysis of zinc-finger nuclease-induced gene targeting in Drosophila. Genetics 182, 641–651 (2009).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    74.Do, A. T., Brooks, J. T., Le Neveu, M. K. & LaRocque, J. R. Double-strand break repair assays determine pathway choice and structure of gene conversion events in Drosophila melanogaster. G3 4, 425–432 (2014).PubMed 
    Article 
    CAS 

    Google Scholar 
    75.Wei, D. S. & Rong, Y. S. A genetic screen for DNA double-strand break repair mutations in Drosophila. Genetics 177, 63–77 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    76.Lin, C. C. & Potter, C. J. Non-Mendelian dominant maternal effects caused by CRISPR/Cas9 transgenic components in Drosophila melanogaster. G3 6, 3685–3691 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    77.Champer, J. et al. Novel CRISPR/Cas9 gene drive constructs reveal insights into mechanisms of resistance allele formation and drive efficiency in genetically diverse populations. PLoS Genet. 13, e1006796 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    78.Anopheles gambiae 1000 Genomes Consortiumet al. Genetic diversity of the African malaria vector Anopheles gambiae. Nature 552, 96–100 (2017).Article 
    CAS 

    Google Scholar 
    79.Deredec, A., Burt, A. & Godfray, H. C. The population genetics of using homing endonuclease genes in vector and pest management. Genetics 179, 2013–2026 (2008).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    80.Fasulo, B. et al. A fly model establishes distinct mechanisms for synthetic CRISPR/Cas9 sex distorters. PLoS Genet. 16, e1008647 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    81.Galizi, R. et al. A synthetic sex ratio distortion system for the control of the human malaria mosquito. Nat. Commun. 5, 3977 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    82.Galizi, R. et al. A CRISPR-Cas9 sex-ratio distortion system for genetic control. Sci. Rep. 6, 31139 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    83.Turner, J. M. Meiotic sex chromosome inactivation. Development 134, 1823–1831 (2007).CAS 
    PubMed 
    Article 

    Google Scholar 
    84.Simoni, A. et al. A male-biased sex-distorter gene drive for the human malaria vector Anopheles gambiae. Nat. Biotechnol. 38, 1054–1060 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    85.Carballar-Lejarazu, R. & et al. Next-generation gene drive for population modification of the malaria vector mosquito, Anopheles gambiae.Proc. Natl Acad. Sci. USA 117, 22805–22814 (2020). This study describes a modification gene drive that propagates with high efficiency through both males and females.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    86.Pham, T. B. et al. Experimental population modification of the malaria vector mosquito, Anopheles stephensi. PLoS Genet. 15, e1008440 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    87.Dong, Y., Simoes, M. L. & Dimopoulos, G. Versatile transgenic multistage effector-gene combinations for Plasmodium falciparum suppression in Anopheles. Sci. Adv. 6, eaay5898 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    88.Dong, Y. et al. Engineered anopheles immunity to Plasmodium infection. PLoS Pathog. 7, e1002458 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    89.Isaacs, A. T. et al. Transgenic Anopheles stephensi coexpressing single-chain antibodies resist Plasmodium falciparum development. Proc. Natl Acad. Sci. USA 109, E1922–E1930 (2012). This study demonstrates 100% protection against parasite transmission in transgenic mosquitoes carrying a dual anti-parasite effector cassette.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    90.Haber, J. E. TOPping off meiosis. Mol. Cell 57, 577–581 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    91.Hammond, A. et al. Regulating the expression of gene drives is key to increasing their invasive potential and the mitigation of resistance. PLoS Genet. 17, e1009321 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    92.Lee, Y. et al. Genome-wide divergence among invasive populations of Aedes aegypti in California. BMC Genomics 20, 204 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    93.Callaway, E. Gene drives thwarted by emergence of resistant organisms. Nature 542, 15 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    94.Unckless, R. L., Clark, A. G. & Messer, P. W. Evolution of resistance against CRISPR/Cas9 gene drive. Genetics 205, 827–841 (2017).PubMed 
    Article 

    Google Scholar 
    95.Drury, D. W., Dapper, A. L., Siniard, D. J., Zentner, G. E. & Wade, M. J. CRISPR/Cas9 gene drives in genetically variable and nonrandomly mating wild populations. Sci. Adv. 3, e1601910 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    96.Schmidt, H. et al. Abundance of conserved CRISPR-Cas9 target sites within the highly polymorphic genomes of Anopheles and Aedes mosquitoes. Nat. Commun. 11, 1425 (2020). This study provides computational evidence that conserved CRISPR cleavage sites are abundant in the genome.CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    97.Akbari, O. S. et al. Safeguarding gene drive experiments in the laboratory. Science 349, 927–929 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    98.Li, J. et al. Genome-block expression-assisted association studies discover malaria resistance genes in Anopheles gambiae. Proc. Natl Acad. Sci. USA 110, 20675–20680 (2013).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    99.Niu, G. et al. The fibrinogen-like domain of FREP1 protein is a broad-spectrum malaria transmission-blocking vaccine antigen. J. Biol. Chem. 292, 11960–11969 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    100.Zhang, G. et al. Anopheles midgut FREP1 mediates plasmodium invasion. J. Biol. Chem. 290, 16490–16501 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    101.Dong, Y., Simoes, M. L., Marois, E. & Dimopoulos, G. CRISPR/Cas9 -mediated gene knockout of Anopheles gambiae FREP1 suppresses malaria parasite infection. PLoS Pathog. 14, e1006898 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    102.Simoes, M. L., Caragata, E. P. & Dimopoulos, G. Diverse host and restriction factors regulate mosquito-pathogen interactions. Trends Parasitol. 34, 603–616 (2018).PubMed 
    Article 

    Google Scholar 
    103.Nash, A. et al. Integral gene drives for population replacement. Biol. Open 8, bio037762 (2019). This study describes a bipartite drive system that can enable testing of anti-parasite effector cassettes under standard mosquito confinement protocols.CAS 
    PubMed 

    Google Scholar 
    104.Enayati, A., Hanafi-Bojd, A. A., Sedaghat, M. M., Zaim, M. & Hemingway, J. Evolution of insecticide resistance and its mechanisms in Anopheles stephensi in the WHO Eastern Mediterranean Region. Malar. J. 19, 258 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    105.Ffrench-Constant, R. H., Williamson, M. S., Davies, T. G. & Bass, C. Ion channels as insecticide targets. J. Neurogenet. 30, 163–177 (2016).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    106.Silva, J. J. & Scott, J. G. Conservation of the voltage-sensitive sodium channel protein within the Insecta. Insect Mol. Biol. 29, 9–18 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    107.Casida, J. E. & Durkin, K. A. Novel GABA receptor pesticide targets. Pestic. Biochem. Physiol. 121, 22–30 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    108.Ihara, M., Buckingham, S. D., Matsuda, K. & Sattelle, D. B. Modes of action, resistance and toxicity of insecticides targeting nicotinic acetylcholine receptors. Curr. Med. Chem. 24, 2925–2934 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    109.Thapa, S., Lv, M. & Xu, H. Acetylcholinesterase: a primary target for drugs and insecticides. Mini Rev. Med. Chem. 17, 1665–1676 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    110.Kleinstiver, B. P. et al. Engineered CRISPR-Cas12a variants with increased activities and improved targeting ranges for gene, epigenetic and base editing. Nat. Biotechnol. 37, 276–282 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    111.Walton, R. T., Christie, K. A., Whittaker, M. N. & Kleinstiver, B. P. Unconstrained genome targeting with near-PAMless engineered CRISPR-Cas9 variants. Science 368, 290–296 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    112.Committee on Gene Drive Research in Non-Human Organisms: Recommendations for Responsible Conduct; Board on Life Sciences; Division on Earth and Life Studies; National Academies of Sciences, Engineering, and Medicine. Gene Drives on the Horizon: Advancing Science, Navigating Uncertainty, and Aligning Research with Public Values (The National Academies Press, 2016). This comprehensive advisory and historical review document summarizes consensus views for how to safely rear and study gene-drive systems in the laboratory.113.Adelman, Z. et al. Rules of the road for insect gene drive research and testing. Nat. Biotechnol. 35, 716–718 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    114.James, S. et al. Pathway to deployment of gene drive mosquitoes as a potential biocontrol tool for elimination of malaria in Sub-Saharan Africa: recommendations of a scientific working group(dagger). Am. J. Trop. Med. Hyg. 98, 1–49 (2018).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    115.James, S. L., Marshall, J. M., Christophides, G. K., Okumu, F. O. & Nolan, T. Toward the definition of efficacy and safety criteria for advancing gene drive-modified mosquitoes to field testing. Vector Borne Zoonotic Dis. 20, 237–251 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    116.Warmbrod, K. L. et al. Gene Drives: Pursuing Opportunities, Minimizing Risk – A Johns Hopkins University Report on Responsible Governance (Johns Hopkins Bloomberg School of Public Health, Center for Health Security, Johns Hopkins University, 2020).117.Vella, M. R., Gunning, C. E., Lloyd, A. L. & Gould, F. Evaluating strategies for reversing CRISPR-Cas9 gene drives. Sci. Rep. 7, 11038 (2017).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    118.Rode, N. O., Courtier-Orgogozo, V. & Debarre, F. Can a population targeted by a CRISPR-based homing gene drive be rescued? G3 10, 3403–3415 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    119.Fedoroff, N., Wessler, S. & Shure, M. Isolation of the transposable maize controlling elements Ac and Ds. Cell 35, 235–242 (1983).CAS 
    PubMed 
    Article 

    Google Scholar 
    120.Paix, A. et al. Precision genome editing using synthesis-dependent repair of Cas9-induced DNA breaks. Proc. Natl Acad. Sci. USA 114, E10745–E10754 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    121.Wu, B., Luo, L. & Gao, X. J. Cas9-triggered chain ablation of cas9 as a gene drive brake. Nat. Biotechnol. 34, 137–138 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    122.Taxiarchi, C. et al. A genetically encoded anti-CRISPR protein constrains gene drive spread and prevents population suppression. Nat. Commun. 12, 3977 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    123.Conklin, B. R. On the road to a gene drive in mammals. Nature 566, 43–45 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    124.Salkeld, D. J. Vaccines for conservation: plague, prairie dogs & black-footed ferrets as a case study. Ecohealth 14, 432–437 (2017).PubMed 
    Article 

    Google Scholar 
    125.Teem, J. L. et al. Genetic biocontrol for invasive species. Front. Bioeng. Biotechnol. 8, 452 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    126.Godwin, J. et al. Rodent gene drives for conservation: opportunities and data needs. Proc. Biol. Sci. 286, 20191606 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    127.McFarlane, G. R., Whitelaw, C. B. A. & Lillico, S. G. CRISPR-based gene drives for pest control. Trends Biotechnol. 36, 130–133 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    128.Klompe, S. E., Vo, P. L. H., Halpin-Healy, T. S. & Sternberg, S. H. Transposon-encoded CRISPR-Cas systems direct RNA-guided DNA integration. Nature 571, 219–225 (2019).CAS 
    PubMed 
    Article 

    Google Scholar 
    129.Koonin, E. V., Makarova, K. S., Wolf, Y. I. & Krupovic, M. Evolutionary entanglement of mobile genetic elements and host defence systems: guns for hire. Nat. Rev. Genet. 21, 119–131 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    130.Strecker, J. et al. RNA-guided DNA insertion with CRISPR-associated transposases. Science 365, 48–53 (2019).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    131.Peters, J. E., Makarova, K. S., Shmakov, S. & Koonin, E. V. Recruitment of CRISPR-Cas systems by Tn7-like transposons. Proc. Natl Acad. Sci. USA 114, E7358–E7366 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    132.Wiegand, T. & Wiedenheft, B. CRISPR Surveillance Turns Transposon Taxi. CRISPR J. 3, 10–12 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    133.Hamilton, T. A. et al. Efficient inter-species conjugative transfer of a CRISPR nuclease for targeted bacterial killing. Nat. Commun. 10, 4544 (2019).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    134.Price, V. J. et al. Enterococcus faecalis CRISPR-cas is a robust barrier to conjugative antibiotic resistance dissemination in the murine intestine. mSphere 4, e00464-19 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    135.Rodrigues, M., McBride, S. W., Hullahalli, K., Palmer, K. L. & Duerkop, B. A. Conjugative delivery of CRISPR-Cas9 for the selective depletion of antibiotic-resistant enterococci. Antimicrob. Agents Chemother. 63, e01454-19 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    136.Carraro, N. et al. Plasmid-like replication of a minimal streptococcal integrative and conjugative element. Microbiology 162, 622–632 (2016).CAS 
    PubMed 
    Article 

    Google Scholar 
    137.Brophy, J. A. N. et al. Engineered integrative and conjugative elements for efficient and inducible DNA transfer to undomesticated bacteria. Nat. Microbiol. 3, 1043–1053 (2018).CAS 
    PubMed 
    Article 

    Google Scholar 
    138.Bikard, D. et al. Exploiting CRISPR-Cas nucleases to produce sequence-specific antimicrobials. Nat. Biotechnol. 32, 1146–1150 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    139.Citorik, R. J., Mimee, M. & Lu, T. K. Sequence-specific antimicrobials using efficiently delivered RNA-guided nucleases. Nat. Biotechnol. 32, 1141–1145 (2014).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    140.Yosef, I., Manor, M., Kiro, R. & Qimron, U. Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc. Natl Acad. Sci. USA 112, 7267–7272 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    141.Park, J. Y. et al. Genetic engineering of a temperate phage-based delivery system for CRISPR/Cas9 antimicrobials against Staphylococcus aureus. Sci. Rep. 7, 44929 (2017).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    142.Pazda, M., Kumirska, J., Stepnowski, P. & Mulkiewicz, E. Antibiotic resistance genes identified in wastewater treatment plant systems – a review. Sci. Total. Env. 697, 134023 (2019).CAS 
    Article 

    Google Scholar 
    143.Kraemer, S. A., Ramachandran, A. & Perron, G. G. Antibiotic pollution in the environment: from microbial ecology to public policy. Microorganisms 7, 180 (2019).CAS 
    PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    144.Ram, G., Ross, H. F., Novick, R. P., Rodriguez-Pagan, I. & Jiang, D. Conversion of staphylococcal pathogenicity islands to CRISPR-carrying antibacterial agents that cure infections in mice. Nat. Biotechnol. 36, 971–976 (2018).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    145.Bier, E. & Nizet, V. Driving to safety: CRISPR-based genetic approaches to reducing antibiotic resistance. Trends Genet. https://doi.org/10.1016/j.tig.2021.02.007 (2021).Article 
    PubMed 

    Google Scholar 
    146.Rossati, A. et al. Climate, environment and transmission of malaria. Infez. Med. 24, 93–104 (2016).PubMed 

    Google Scholar 
    147.Fontenille, D. & Powell, J. R. From anonymous to public enemy: how does a mosquito become a feared arbovirus vector? Pathogens 9, 265 (2020).PubMed Central 
    Article 
    PubMed 

    Google Scholar 
    148.Lidani, K. C. F. et al. Chagas disease: from discovery to a worldwide health problem. Front. Public Health 7, 166 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    149.Buscher, P., Cecchi, G., Jamonneau, V. & Priotto, G. Human African trypanosomiasis. Lancet 390, 2397–2409 (2017).PubMed 
    Article 

    Google Scholar 
    150.Desjeux, P. Leishmaniasis: current situation and new perspectives. Comp. Immunol. Microbiol. Infect. Dis. 27, 305–318 (2004).CAS 
    PubMed 
    Article 

    Google Scholar 
    151.Saxena, V., Bolling, B. G. & Wang, T. West nile virus. Clin. Lab. Med. 37, 243–252 (2017).PubMed 
    Article 

    Google Scholar 
    152.Simon, L. V., Kong, E. L. & Graham, C. in St. Louis Encephalitis (StatPearls, 2020).153.Feng, X. et al. Optimized CRISPR tools and site-directed transgenesis towards gene drive development in Culex quinquefasciatus mosquitoes. Nat. Commun. 12, 2960 (2021).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    154.Nepomichene, T. N., Andrianaivolambo, L., Boyer, S. & Bourgouin, C. Efficient method for establishing F1 progeny from wild populations of Anopheles mosquitoes. Malar. J. 16, 21 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    155.Marchand, R. P. A new cage for observing mating behavior of wild Anopheles gambiae in the laboratory. J. Am. Mosq. Control. Assoc. 1, 234–236 (1985).CAS 
    PubMed 

    Google Scholar 
    156.Nunes-da-Fonseca, R., Berni, M., Tobias-Santos, V., Pane, A. & Araujo, H. M. Rhodnius prolixus: from classical physiology to modern developmental biology. Genesis https://doi.org/10.1002/dvg.22995 (2017).Article 
    PubMed 

    Google Scholar 
    157.Chaverra-Rodriguez, D. et al. Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat. Commun. 9, 3008 (2018).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    158.Macias, V. M. et al. Cas9-mediated gene-editing in the malaria mosquito anopheles stephensi by ReMOT Control. G3 10, 1353–1360 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    159.Chaverra-Rodriguez, D. et al. Germline mutagenesis of Nasonia vitripennis through ovarian delivery of CRISPR-Cas9 ribonucleoprotein. Insect Mol. Biol. 29, 569–577 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    160.Heu, C. C., McCullough, F. M., Luan, J. & Rasgon, J. L. CRISPR-Cas9-based genome editing in the silverleaf whitefly (Bemisia tabaci). CRISPR J. 3, 89–96 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    161.Prowse, T. A., Adikusuma, F., Cassey, P., Thomas, P. & Ross, J. V. A Y-chromosome shredding gene drive for controlling pest vertebrate populations. eLife 8, e41873 (2019).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    162.Carballar-Lejarazu, R. & James, A. A. Population modification of Anopheline species to control malaria transmission. Pathog. Glob. Health 111, 424–435 (2017).PubMed 
    Article 
    PubMed Central 

    Google Scholar 
    163.Annas, G. J. et al. A code of ethics for gene drive research. CRISPR J. 4, 19–24 (2021).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    164.Bier, E. & Sober, E. Gene editing and the war against malaria. Am. Sci. 108, 162–169 (2020).Article 

    Google Scholar 
    165.Long, K. C. et al. Core commitments for field trials of gene drive organisms. Science 370, 1417–1419 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    166.Kormos, A. et al. Application of the relationship-based model to engagement for field trials of genetically engineered malaria vectors.Am. J. Trop. Med. Hyg. 104, 805–811 (2020).PubMed Central 
    PubMed 

    Google Scholar 
    167.World Health Organization. Guidance framework for testing of genetically modified mosquitoes. WHO http://apps.who.int/iris/bitstream/10665/127889/1/9789241507486_eng.pdf (2014).168.Smith, D. L., McKenzie, F. E., Snow, R. W. & Hay, S. I. Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 5, e42 (2007).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    169.Brauer, F., Castillo-Chavez, C., Mubayi, A. & Towers, S. Some models for epidemics of vector-transmitted diseases. Infect. Dis. Model. 1, 79–87 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    170.Deredec, A., Godfray, H. C. & Burt, A. Requirements for effective malaria control with homing endonuclease genes. Proc. Natl Acad. Sci. USA 108, E874–E880 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    171.Escalante, A. A. & Pacheco, M. A. Malaria molecular epidemiology: an evolutionary genetics perspective. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.AME-0010-2019 (2019).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    172.Selvaraj, P. et al. Vector genetics, insecticide resistance and gene drives: An agent-based modeling approach to evaluate malaria transmission and elimination. PLoS Comput. Biol. 16, e1008121 (2020).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar  More

  • in

    Metagenomic approaches reveal differences in genetic diversity and relative abundance of nitrifying bacteria and archaea in contrasting soils

    1.Spiertz, J. H. J. Nitrogen, sustainable agriculture and food security: a review. Agron. Sustain. Dev. 30, 43–55. https://doi.org/10.1051/agro:2008064 (2010).CAS 
    Article 

    Google Scholar 
    2.Kowalchuk, G. A. & Stephen, J. R. Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu. Rev. Microbiol. 55, 485–529. https://doi.org/10.1146/annurev.micro.55.1.485 (2001).CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Zumft, W. G. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61, 533–616 (1997).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    4.Gelfand, I. & Yakir, D. Influence of nitrite accumulation in association with seasonal patterns and mineralization of soil nitrogen in a semi-arid pine forest. Soil Biol. Biochem. 40, 415–424. https://doi.org/10.1016/j.soilbio.2007.09.005 (2008).CAS 
    Article 

    Google Scholar 
    5.Subbarao, G. V. et al. Scope and strategies for regulation of nitrification in agricultural systems-challenges and opportunities. Crit. Rev. Plant Sci. 25, 303–335. https://doi.org/10.1080/07352680600794232 (2006).CAS 
    Article 

    Google Scholar 
    6.Shen, T., Stieglmeier, M., Dai, J., Urich, T. & Schleper, C. Responses of the terrestrial ammonia-oxidizing archaeon Ca. Nitrososphaera viennensis and the ammonia-oxidizing bacterium Nitrosospira multiformis to nitrification inhibitors. FEMS Microbiol. Lett. 344, 121–129, https://doi.org/10.1111/1574-6968.12164 (2013).7.Prosser, J. I., Head, I. M. & Stein, L. Y. in The Prokaryotes – Alphaproteobacteria and Betaproteobacteria (ed DeLong Rosenberg E., E.F., Lory, S., Stackebrandt, E., Thompson, F.) 901–918 (Springer-Verlag, 2014).8.Hayatsu, M. et al. An acid-tolerant ammonia-oxidizing gamma-proteobacterium from soil. ISME J. 11, 1130–1141. https://doi.org/10.1038/ismej.2016.191 (2017).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    9.Alves, R.J.E., Minh, B.Q, Urich, T., von Haeseler, A. & Schleper, C. Unifying the global phylogeny and environmental distribution of ammonia-oxidising archaea based on amoA genes. Nat. Commun. 9, https://doi.org/10.1038/s41467-018-03861-1 (2018).10.Wang, H. Et al. Distinct distribution of archaea from soil to freshwater to estuary: implications of archaeal composition and function in different environments. Front. Microbiol. 11. https://doi.org/10.3389/fmicb.2020.576661 (2020).11.Prosser, J. I. & Nicol, G. W. Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol. 20, 523–531. https://doi.org/10.1016/j.tim.2012.08.001 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    12.Pester, M. et al. amoA-based consensus phylogeny of ammonia-oxidizing archaea and deep sequencing of amoA genes from soils of four different geographic regions. Environ. Microbiol. 14, 525–539. https://doi.org/10.1111/j.1462-2920.2011.02666.x (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    13.Spang, A. et al. The genome of the ammonia-oxidizing Candidatus Nitrososphaera gargensis: insights into metabolic versatility and environmental adaptations. Environ. Microbiol. 14, 3122–3145. https://doi.org/10.1111/j.1462-2920.2012.02893.x (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    14.Daims, H. et al. Complete nitrification by Nitrospira bacteria. Nature 528, 504–509. https://doi.org/10.1038/nature16461 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    15.van Kessel, M. A. et al. Complete nitrification by a single microorganism. Nature 528, 555–559. https://doi.org/10.1038/nature16459 (2015).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    16.Junier, P. et al. Phylogenetic and functional marker genes to study ammonia-oxidizing microorganisms (AOM) in the environment. Appl. Microbiol. Biotechnol. 85, 425–440. https://doi.org/10.1007/s00253-009-2228-9 (2010).CAS 
    Article 
    PubMed 

    Google Scholar 
    17.Leininger, S. et al. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442, 806–809. https://doi.org/10.1038/nature04983 (2006).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    18.Zhalnina, K. et al. Ca. Nitrososphaera and Bradyrhizobium are inversely correlated and related to agricultural practices in long-term field experiments. Front. Microbiol. 4, 104, https://doi.org/10.3389/fmicb.2013.00104 (2013).19.Pjevac, P. et al. AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammox Nitrospira in the environment. Front. Microbiol. 8, 1508. https://doi.org/10.3389/fmicb.2017.01508 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    20.Palomo, A., Dechesne, A. & Smets, B. F. Genomic profiling of Nitrospira species reveals ecological success of comammox Nitrospira. bioRxiv, 612226, https://doi.org/10.1101/612226 (2019).21.Poghosyan, L. et al. Metagenomic recovery of two distinct comammox Nitrospira from the terrestrial subsurface. Environ. Microbiol. 21, 3627–3637. https://doi.org/10.1111/1462-2920.14691 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    22.Palomo, A. et al. Comparative genomics sheds light on niche differentiation and the evolutionary history of comammox Nitrospira. ISME J. 12, 1779–1793. https://doi.org/10.1038/s41396-018-0083-3 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    23.Strous, M. et al. Deciphering the evolution and metabolism of an anammox bacterium from a community genome. Nature 440, 790–794. https://doi.org/10.1038/nature04647 (2006).ADS 
    Article 
    PubMed 

    Google Scholar 
    24.De Boer, W. & Kowalchuk, G. A. Nitrification in acid soils: micro-organisms and mechanisms. Soil Biol. Biochem. 33, 853–866. https://doi.org/10.1016/s0038-0717(00)00247-9 (2001).Article 

    Google Scholar 
    25.Tourna, M. et al. Nitrososphaera viennensis, an ammonia oxidizing archaeon from soil. Proc. Natl. Acad. Sci. USA. 108, 8420–8425. https://doi.org/10.1073/pnas.1013488108 (2011).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    26.Arp, D. J., Chain, P. S. G. & Klotz, M. G. The impact of genome analyses on our understanding of ammonia-oxidizing bacteria. Annu. Rev. Microbiol. 61, 503–528 (2007).CAS 
    Article 

    Google Scholar 
    27.Simon, J. & Klotz, M. G. Diversity and evolution of bioenergetic systems involved in microbial nitrogen compound transformations. Biochim. Biophys. Acta 114–135, 2013. https://doi.org/10.1016/j.bbabio.2012.07.005 (1827).CAS 
    Article 

    Google Scholar 
    28.Walker, C. B. et al. Nitrosopumilus maritimus genome reveals unique mechanisms for nitrification and autotrophy in globally distributed marine crenarchaea. Proc. Natl. Acad. Sci. USA 107, 8818–8823. https://doi.org/10.1073/pnas.0913533107 (2010).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    29.Li, C. Y., Hu, H. W., Chen, Q. L., Chen, D. L. & He, J. Z. Comammox Nitrospira play an active role in nitrification of agricultural soils amended with nitrogen fertilizers. Soil Biol. Biochem. 138, https://doi.org/10.1016/j.soilbio.2019.107609 (2019).30.Li, C. Y., Hu, H. W., Chen, Q. L., Chen, D. L. & He, J. Z. Niche differentiation of clade A comammox Nitrospira and canonical ammonia oxidizers in selected forest soils. Soil Biol. Biochem. 149, https://doi.org/10.1016/j.soilbio.2020.107925 (2020).31.Daims, H., Lucker, S. & Wagner, M. A new perspective on microbes formerly known as nitrite-oxidizing bacteria. Trends Microbiol. 24, 699–712. https://doi.org/10.1016/j.tim.2016.05.004 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Castelle, C. J. et al. Extraordinary phylogenetic diversity and metabolic versatility in aquifer sediment. Nat. Commun. 4, 2120. https://doi.org/10.1038/ncomms3120 (2013).ADS 
    Article 
    PubMed 

    Google Scholar 
    33.Sorokin, D. Y. et al. Nitrification expanded: discovery, physiology and genomics of a nitrite-oxidizing bacterium from the phylum Chloroflexi. ISME J. 6, 2245–2256. https://doi.org/10.1038/ismej.2012.70 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    34.Lucker, S. et al. A Nitrospira metagenome illuminates the physiology and evolution of globally important nitrite-oxidizing bacteria. Proc. Natl. Acad. Sci. USA. 107, 13479–13484. https://doi.org/10.1073/pnas.1003860107 (2010).ADS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    35.Mendum, T. A., Sockett, R. E. & Hirsch, P. R. Use of molecular and isotopic techniques to monitor the response of autotrophic ammonia-oxidizing populations of the beta subdivision of the class Proteobacteria in arable soils to nitrogen fertilizer. Appl. Environ. Microbiol. 65, 4155–4162 (1999).ADS 
    CAS 
    Article 

    Google Scholar 
    36.Hirsch, P. R. et al. Soil resilience and recovery: rapid community responses to management changes. Plant Soil 412, 283–297. https://doi.org/10.1007/s11104-016-3068-x (2017).CAS 
    Article 
    PubMed 

    Google Scholar 
    37.Hirsch, P. R., Mauchline, T. H. & Clark, I. M. Culture-independent molecular techniques for soil microbial ecology. Soil Biol. Biochem. 42, 878–887. https://doi.org/10.1016/j.soilbio.2010.02.019 (2010).CAS 
    Article 

    Google Scholar 
    38.Vetrovsky, T. & Baldrian, P. The variability of the 16S rRNA gene in bacterial genomes and its consequences for bacterial community analyses. PLoS ONE 8, e57923. https://doi.org/10.1371/journal.pone.0057923 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    39.Fu, Q.L., Clark, I.M., Zhu, J., Hu, H.Q. & Hirsch, P.R The short-term effects of nitrification inhibitors on the abundance and expression of ammonia. and nitrite oxidizers in a long-term field experiment comparing land management. Biol Fertil Soils. 54, 163–172. https://doi.org/10.1007/s00374-017-1249-2 (2018).40.Bollmann, A., Schmidt, I., Saunders, A. M. & Nicolaisen, M. H. Influence of starvation on potential ammonia-oxidizing activity and amoA mRNA levels of Nitrosospira briensis. Appl. Environ. Microbiol. 71, 1276–1282. https://doi.org/10.1128/aem.71.3.1276-1282.2005 (2005).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    41.Li, C. Y., Hu, H. W., Chen, Q. L., Chen, D. L. & He, J. Z. Growth of comammox Nitrospira is inhibited by nitrification inhibitors in agricultural soils. J. Soils Sediments 20, 621–628. https://doi.org/10.1007/s11368-019-02442-z (2020).CAS 
    Article 

    Google Scholar 
    42.Koch, H., van Kessel, M. A. H. J. & Lücker, S. Complete nitrification: insights into the ecophysiology of comammox Nitrospira. Appl. Microbiol. Biotechnol. 103, 177–189. https://doi.org/10.1007/s00253-018-9486-3 (2019).CAS 
    Article 
    PubMed 

    Google Scholar 
    43.Placella, S. A. & Firestone, M. K. Transcriptional response of nitrifying communities to wetting of dry soil. Appl. Environ. Microbiol. 79, 3294–3302. https://doi.org/10.1128/AEM.00404-13 (2013).ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    44.Hirsch, P. R. et al. Starving the soil of plant inputs for 50 years reduces abundance but not diversity of soil bacterial communities. Soil Biol. Biochem. 41, 2021–2024. https://doi.org/10.1016/j.soilbio.2009.07.011 (2009).CAS 
    Article 

    Google Scholar 
    45.Clark, I. M., Buchkina, N., Jhurreea, D., Goulding, K. W. & Hirsch, P. R. Impacts of nitrogen application rates on the activity and diversity of denitrifying bacteria in the Broadbalk Wheat Experiment. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1235–1244, https://doi.org/10.1098/rstb.2011.0314 (2012).46.Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. Nat. Meth. 12, 59–60 (2015).CAS 
    Article 

    Google Scholar 
    47.Huson, D. H., Auch, A. F., Qi, J. & Schuster, S. C. MEGAN analysis of metagenomic data. Genome Res. 17, 377–386. https://doi.org/10.1101/gr.5969107 (2007).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    48.Katoh, K. & Standley, D. M. MAFFT Multiple Sequence Alignment Software Version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. https://doi.org/10.1093/molbev/mst010 (2013).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar  More

  • in

    The phyllosphere microbiome of host trees contributes more than leaf phytochemicals to variation in the Agrilus planipennis Fairmaire gut microbiome structure

    1.Feldhaar, H. Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol. Entomol. 36, 533–543 (2011).Article 

    Google Scholar 
    2.Popa, V., Deziel, E., Lavallee, R., Bauce, E. & Guertin, C. The complex symbiotic relationships of bark beetles with microorganisms: A potential practical approach for biological control in forestry. Pest Manag. Sci. 68, 963–975. https://doi.org/10.1002/ps.3307 (2012).CAS 
    Article 
    PubMed 

    Google Scholar 
    3.Qadri, M., Short, S., Gast, K., Hernandez, J. & Wong, A.C.-N. Microbiome innovation in agriculture: Development of microbial based tools for insect pest management. Front. Sustain. Food Syst. 4, 547751. https://doi.org/10.3389/fsufs (2020).Article 

    Google Scholar 
    4.Vasanthakumar, A., Handelsman, J., Schloss, P. D., Bauer, L. S. & Raffa, K. F. Gut microbiota of an invasive subcortical beetle, Agrilus planipennis Fairmaire, across various life stages. Environ. Entomol. 37, 1344–1353 (2008).PubMed 
    Article 

    Google Scholar 
    5.Zhang, Z., Jiao, S., Li, X. & Li, M. Bacterial and fungal gut communities of Agrilus mali at different developmental stages and fed different diets. Sci. Rep. 8, 15634. https://doi.org/10.1038/s41598-018-34127-x (2018).CAS 
    Article 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    6.Franzini, P. Z., Ramond, J.-B., Scholtz, C. H., Sole, C. L., Ronca, S. & Cowan, D. A. The gut microbiomes of two Pachysoma MacLeay desert dung beetle species (Coleoptera: Scarabaeidae: Scarabaeinae) feeding on different diets. PLoS ONE 11, e0161118 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    7.Colman, D. R., Toolson, E. C. & Takacs-Vesbach, C. Do diet and taxonomy influence insect gut bacterial communities?. Mol. Ecol. 21, 5124–5137 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    8.Kim, J. M. Choi, M.-Y., Kim, J.-W., Lee, S. A., Ahn, J.-H., Song, J., Kim, S.-H. & Weon, H.-Y. Effects of diet type, developmental stage, and gut compartment in the gut bacterial communities of two Cerambycidae species (Coleoptera). J. Microbiol. 55, 21–30 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    9.Ferguson, L. V.  Dhakal, P., Lebenzon, J. E., Heinrichs, D. E., Bucking, C., & Sinclair B. J. Seasonal shifts in the insect gut microbiome are concurrent with changes in cold tolerance and immunity. Funct. Ecol. 32, 2357–2368 (2018).Article 

    Google Scholar 
    10.Mason, C. J., Hanshew, A. S. & Raffa, K. F. Contributions by host trees and insect activity to bacterial communities in Dendroctonus valens (Coleoptera: Curculionidae) galleries, and their high overlap with other microbial assemblages of bark beetles. Environ. Entomol. 45, 348–356. https://doi.org/10.1093/ee/nvv184 (2015).CAS 
    Article 
    PubMed 

    Google Scholar 
    11.Mogouong, J., Constant, P., Lavallée, R. & Guertin, C. Gut microbiome of the emerald ash borer, Agrilus planipennis Fairmaire, and its relationship with insect population density. FEMS Microbiol. Ecol. https://doi.org/10.1093/femsec/fiaa141 (2020).Article 
    PubMed 

    Google Scholar 
    12.Moran, N. A. & Yun, Y. Experimental replacement of an obligate insect symbiont. Proc. Natl. Acad. Sci. 112, 2093–2096 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    13.Borcard, D., Legendre, P. & Drapeau, P. Partialling out the spatial component of ecological variation. Ecology 73, 1045–1055 (1992).Article 

    Google Scholar 
    14.Peres-Neto, P. R., Legendre, P., Dray, S. & Borcard, D. Variation partitioning of species data matrices: Estimation and comparison of fractions. Ecology 87, 2614–2625 (2006).PubMed 
    Article 

    Google Scholar 
    15.Cappaert, D., McCullough, D. G., Poland, T. M. & Siegert, N. W. Emerald ash borer in North America: A research and regulatory challenge. (2005).16.Kovacs, K. F., Haight, R. G., McCullough, D. G., Mercader, R. J., Siegert, N. W. & Liebhold, A. M. Cost of potential emerald ash borer damage in U.S. communities, 2009–2019. Ecol. Econ. 69, 569–578 (2010).Article 

    Google Scholar 
    17.Aukema, J. E., Leung, B., Kovacs, K., Chivers, C., Britton, K. O., Englin, J., Frankel, S. J., Haight, R. G., Holmes, T. P., Liebhold, A. M., McCullough, D. G. & Von Holle, B. Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6, e24587 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    18.Poland, T. M. & McCullough, D. G. Emerald ash borer: Invasion of the urban forest and the threat to North America’s ash resource. J. For. 104, 118–124 (2006).
    Google Scholar 
    19.Herms, D. A. & McCullough, D. G. Emerald ash borer invasion of North America: History, biology, ecology, impacts, and management. Annu. Rev. Entomol. 59, 13–30. https://doi.org/10.1146/annurev-ento-011613-162051 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    20.McCullough, D. G. Challenges, tactics and integrated management of emerald ash borer in North America. For. Int. J. For. Res. 93, 197–211 (2020).
    Google Scholar 
    21.Gandhi, K. J. & Herms, D. A. North American arthropods at risk due to widespread Fraxinus mortality caused by the alien emerald ash borer. Biol. Invasions 12, 1839–1846 (2010).Article 

    Google Scholar 
    22.Slesak, R. A., Lenhart, C. F., Brooks, K. N., D’Amato, A. W. & Palik, B. J. Water table response to harvesting and simulated emerald ash borer mortality in black ash wetlands in Minnesota, USA. Can. J. For. Res. 44, 961–968 (2014).Article 

    Google Scholar 
    23.Wielkopolan, B. & Obrepalska-Steplowska, A. Three-way interaction among plants, bacteria, and coleopteran insects. Planta 244, 313–332. https://doi.org/10.1007/s00425-016-2543-1 (2016).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    24.Howe, G. A. & Jander, G. Plant immunity to insect herbivores. Annu. Rev. Plant Biol. 59, 41–66 (2008).CAS 
    PubMed 
    Article 

    Google Scholar 
    25.Stam, J. M., Kroes, A., Li, Y., Gols, R., van Loon, J. J. A., Poelman, E. H. & Dicke, M. Plant interactions with multiple insect herbivores: from community to genes. Annu. Rev. Plant Biol. 65, 689–713 (2014).CAS 
    PubMed 
    Article 

    Google Scholar 
    26.Douglas, A. E. Multiorganismal insects: Diversity and function of resident microorganisms. Annu. Rev. Entomol. 60, 17–34 (2015).CAS 
    PubMed 
    Article 

    Google Scholar 
    27.Vorholt, J. A. Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828 (2012).CAS 
    PubMed 
    Article 

    Google Scholar 
    28.Shikano, I., Rosa, C., Tan, C.-W. & Felton, G. W. Tritrophic interactions: Microbe-mediated plant effects on insect herbivores. Annu. Rev. Phytopathol. 55, 313–331 (2017).CAS 
    PubMed 
    Article 

    Google Scholar 
    29.Schowalter, T. D. Insect Ecology: An Ecosystem Approach (Academic Press, 2016).
    Google Scholar 
    30.Oliverio, A. M., Gan, H., Wickings, K. & Fierer, N. A DNA metabarcoding approach to characterize soil arthropod communities. Soil Biol. Biochem. 125, 37–43 (2018).CAS 
    Article 

    Google Scholar 
    31.Lennon, J. T., Muscarella, M. E., Placella, S. A. & Lehmkuhl, B. K. How, when, and where relic DNA affects microbial diversity. MBio 9, e00637-e618. https://doi.org/10.1128/mBio.00637-18 (2018).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    32.Humphrey, P. T. & Whiteman, N. K. Insect herbivory reshapes a native leaf microbiome. Nat. Ecol. Evol. 4, 221–229 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    33.Yutthammo, C., Thongthammachat, N., Pinphanichakarn, P. & Luepromchai, E. Diversity and activity of PAH-degrading bacteria in the phyllosphere of ornamental plants. Microb. Ecol. 59, 357–368 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    34.Kadivar, H. & Stapleton, A. E. Ultraviolet radiation alters maize phyllosphere bacterial diversity. Microb. Ecol. 45, 353–361 (2003).CAS 
    PubMed 
    Article 

    Google Scholar 
    35.Thapa, S. & Prasanna, R. Prospecting the characteristics and significance of the phyllosphere microbiome. Ann. Microbiol. 68, 229–245 (2018).CAS 
    Article 

    Google Scholar 
    36.Kembel, S. W., O’Connor, T. K., Arnold, H. K., Hubbell, S. P., Wright, S. J. & Green, J. L. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc. Natl. Acad. Sci. 111, 13715–13720 (2014).37.Biedermann, P. H. & Vega, F. E. Ecology and evolution of insect–fungus mutualisms. Annu. Rev. Entomol. 65, 431–455 (2020).CAS 
    PubMed 
    Article 

    Google Scholar 
    38.Fischer, R., Ostafe, R. & Twyman, R. M. In: Yellow Biotechnology II: Insect Biotechnology in Plant Protection and Industry. Ch. Cellulases from insects, 51–64 (Springer, 2013).39.Watanabe, H. & Tokuda, G. Cellulolytic systems in insects. Ann. Rev. Entomol. 55, 609–632 (2010).CAS 
    Article 

    Google Scholar 
    40.Mittapalli, O., Bai, X., Mamidala, P., Rajarapu, S. P., Bonello, P. & Herms, D. A. Tissue-specific transcriptomics of the exotic invasive insect pest emerald ash borer (Agrilus planipennis). PLoS ONE 5, e13708 (2010).PubMed 
    PubMed Central 
    Article 
    ADS 
    CAS 

    Google Scholar 
    41.Vacheron, J., Péchy-Tarr, M., Brochet, S., Heiman, C. M., Stojiljkovic, M., Maurhofer, M. & Keel, C. T6SS contributes to gut microbiome invasion and killing of an herbivorous pest insect by plant-beneficial Pseudomonas protegens. ISME J. 13, 1318–1329. https://doi.org/10.1038/s41396-019-0353-8 (2019).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    42.Smith, C. C., Snowberg, L. K., Caporaso, J. G., Knight, R. & Bolnick, D. I. Dietary input of microbes and host genetic variation shape among-population differences in stickleback gut microbiota. ISME J. 9, 2515–2526 (2015).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    43.Agler, M. T., Ruhe, J., Kroll, S., Morhenn, C., Kim, S.-T., Weigel, D. & Kemen, E. M. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016).PubMed 
    PubMed Central 
    Article 
    CAS 

    Google Scholar 
    44.Gupta, A. & Nair, S. Dynamics of insect-microbiome interaction influence host and microbial symbiont. Front. Microbiol. 11, 1357 (2020).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    45.AFSQ. La clé forestière. https://afsq.org/cle-forestiere/accueil.html. Association forestière du Sud du Québec (2018).46.Comeau, A. M., Li, W. K. W., Tremblay, J. -É., Carmack, E. C. & Lovejoy, C. Arctic Ocean Microbial Community Structure before and after the 2007 Record Sea Ice Minimum. PLoS ONE 6, e27492. https://doi.org/10.1371/journal.pone.0027492 (2011).CAS 
    Article 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    47.Toju, H., Tanabe, A. S., Yamamoto, S. & Sato, H. High-coverage ITS primers for the DNA-based identification of ascomycetes and basidiomycetes in environmental samples. PLoS ONE 7, e40863. https://doi.org/10.1371/journal.pone.0040863 (2012).CAS 
    Article 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 
    48.Edgar, R. C. UNOISE2: Improved error-correction for Illumina 16S and ITS amplicon sequencing. BioRxiv 081257 (2016).49.Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    50.Callahan, B. J., McMurdie, P. J. & Holmes, S. P. Exact sequence variants should replace operational taxonomic units in marker-gene data analysis. ISME J. 11, 2639 (2017).PubMed 
    PubMed Central 
    Article 

    Google Scholar 
    51.Glassman, S. I. & Martiny, J. B. H. Broadscale ecological patterns are robust to use of exact sequence variants versus operational taxonomic units. mSphere 3, e00148-e118. https://doi.org/10.1128/mSphere.00148-18 (2018).CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    52.Cole, J. R., Wang, Q., Fish, J. A., Chai, B., McGarrell, D. M., Sun, Y.,  Brown, C. T.,  Porras-Alfaro, A., Kuske, C. R. & Tiedje J. M. Ribosomal database project: Data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633-642. https://doi.org/10.1093/nar/gkt1244 (2014).CAS 
    Article 
    PubMed 

    Google Scholar 
    53.Wang, Q., Garrity, G. M., Tiedje, J. M. & Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261–5267 (2007).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    54.Chen, Y. & Poland, T. M. Interactive influence of leaf age, light intensity, and girdling on green ash foliar chemistry and emerald ash borer development. J. Chem. Ecol. 35, 806–815. https://doi.org/10.1007/s10886-009-9661-1 (2009).CAS 
    Article 
    PubMed 

    Google Scholar 
    55.Bi, J. L., Toscano, N. C. & Madore, M. A. Effect of urea fertilizer application on soluble protein and free amino acid content of cotton petioles in relation to silverleaf whitefly (Bemisia argentifolii) populations. J. Chem. Ecol. 29, 747–761. https://doi.org/10.1023/a:1022880905834 (2003).CAS 
    Article 
    PubMed 

    Google Scholar 
    56.Torti, S. D., Dearing, M. D. & Kursar, T. A. Extraction of phenolic compounds from fresh leaves: A comparison of methods. J. Chem. Ecol. 21, 117–125 (1995).CAS 
    PubMed 
    Article 

    Google Scholar 
    57.Hagerman, A. E. Extraction of tannin from fresh and preserved leaves. J. Chem. Ecol. 14, 453–461 (1988).CAS 
    PubMed 
    Article 

    Google Scholar 
    58.Beauchemin, N. J., Furnholm,T., Lavenus, J., Svistoonoff, S., Doumas, P., Bogusz, D., Laplaze, L. & Tisa L. S. Casuarina root exudates alter the physiology, surface properties, and plant infectivity of Frankia sp. strain CcI3. Appl. Environ. Microbiol. 78, 575–580 (2012).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    59.Garg, B. Plant Analysis: Comprehensive Methods and Protocols (Scientific Publishers, 2012).
    Google Scholar 
    60.Wellburn, R. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144, 307–313 (1994).CAS 
    Article 

    Google Scholar 
    61.Marquis, R. J., Newell, E. A. & Villegas, A. C. Non-structural carbohydrate accumulation and use in an understorey rain-forest shrub and relevance for the impact of leaf herbivory. Funct. Ecol. 11, 636–643. https://doi.org/10.1046/j.1365-2435.1997.00139.x (1997).Article 

    Google Scholar 
    62.Garcia, A. M. N., Moumen, A., Ruiz, D. Y. & Alcaide, E. M. Chemical composition and nutrients availability for goats and sheep of two-stage olive cake and olive leaves. Anim. Feed Sci. Technol. 107, 61–74 (2003).Article 
    CAS 

    Google Scholar 
    63.Van Soest, P. V., Robertson, J. & Lewis, B. Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J. Dairy Sci. 74, 3583–3597 (1991).PubMed 
    Article 

    Google Scholar 
    64.Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, D., Minchin, P. R. & O’Hara, R. B. Package ‘vegan’. R package version 2.5-6 (2019)65.Borcard, D., Gillet, F. & Legendre, P. Numerical Ecology with R (Springer, 2018).MATH 
    Book 

    Google Scholar 
    66.Kembel, S. W., Eisen, J. A., Pollard, K. S. & Green, J. L. The phylogenetic diversity of metagenomes. PLoS ONE 6, e23214 (2011).CAS 
    PubMed 
    PubMed Central 
    Article 
    ADS 

    Google Scholar 
    67.Faith, D. P. Conservation evaluation and phylogenetic diversity. Biol. Cons. 61, 1–10 (1992).Article 

    Google Scholar 
    68.Kembel, S. W.,  Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., Ackerly, D. D., Blomberg, S. P., & Webb, C. O. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010).CAS 
    PubMed 
    Article 

    Google Scholar 
    69.Legendre, P. & De Cáceres, M. Beta diversity as the variance of community data: Dissimilarity coefficients and partitioning. Ecol. Lett. 16, 951–963 (2013).PubMed 
    Article 

    Google Scholar 
    70.Dray, S., Bauman, D., Blanchet, G., Borcard, D., Clappe, S., Guenard, G., Jombart, T., Larocque, G., Legendre, P., Madi, N, Wagner H. H. Package ‘adespatial’, version 0.3-14. R Package version 2.5.6 (2018).71.De Cáceres, M., Legendre, P. & Moretti, M. Improving indicator species analysis by combining groups of sites. Oikos 119, 1674–1684 (2010).Article 

    Google Scholar 
    72.De Caceres, M., Jansen, F. & Caceres, D. Package ‘indicspecies’, version 1.7.9. R package version 2.5.6 (2016).73.Blanchet, F. G., Legendre, P. & Borcard, D. Forward selection of explanatory variables. Ecology 89, 2623–2632 (2008).PubMed 
    Article 

    Google Scholar  More

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    Ghostly conduits

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    Bird–plant dispersal limits

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