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    Coastal upwelling generates cryptic temperature refugia

    Ackerly, D. D. et al. The geography of climate change: Implications for conservation biogeography. Divers. Distrib. 16, 476–487 (2010).
    Google Scholar 
    Lawton, J. H. Are there general laws in ecology?. Oikos 84, 177–192 (1999).
    Google Scholar 
    Simberloff, D. Community ecology: Is it time to move on?. Am. Nat. 163, 787–799 (2004).PubMed 

    Google Scholar 
    Ricklefs, R. E. Disintegration of the ecological community. Am. Nat. 172, 741–750 (2008).PubMed 

    Google Scholar 
    McGill, B. J. et al. Species abundance distributions: Moving beyond single prediction theories to integration within an ecological framework. Ecol. Lett. 10, 995–1015 (2007).PubMed 

    Google Scholar 
    Paine, R. T. The Pisaster-Tegula interaction: Prey patches, predator food preference, and intertidal community structure. Ecology 50, 950–961 (1969).
    Google Scholar 
    Dayton, P. K. Competition, disturbance, and community organization: The provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41, 351–389 (1971).
    Google Scholar 
    Hairston, N. G., Smith, F. E. & Slobodkin, L. B. Community structure, population control, and competition. Am. Nat. 94, 421–425 (1960).
    Google Scholar 
    Brose, U., Berlow, E. L. & Martinez, N. D. Scaling up keystone effects from simple to complex ecological networks. Ecol. Lett. 8, 1317–1325 (2005).
    Google Scholar 
    Stouffer, D. B. & Bascompte, J. Understanding food-web persistence from local to global scales. Ecol. Lett. 13, 154–161 (2010).PubMed 

    Google Scholar 
    Loreau, M., Mouquet, N. & Gonzalez, A. Biodiversity as spatial insurance in heterogeneous landscapes. Proc. Natl. Acad. Sci. 100, 12765–12770 (2003).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Leibold, M. A. et al. The metacommunity concept: A framework for multi-scale community ecology. Ecol. Lett. 7, 601–613 (2004).
    Google Scholar 
    Holyoak, M., Leibold, M. A. & Holt, R. D. Metacommunities: Spatial Dynamics and Ecological Communities (University of Chicago Press, 2005).
    Google Scholar 
    Gotelli, N. J. Macroecological signals of species interactions in the Danish avifauna. Proc. Natl. Acad. Sci. USA. 107, 5030–5035 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gouhier, T. C., Guichard, F. & Menge, B. A. Ecological processes can synchronize marine population dynamics over continental scales. Proc. Natl. Acad. Sci. 107, 8281–8286 (2010).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Salois, S. L., Gouhier, T. C. & Menge, B. A. The multifactorial effects of dispersal on biodiversity in environmentally forced metacommunities. Ecosphere 9, e02357 (2018).
    Google Scholar 
    Helmuth, B. et al. Beyond long-term averages: Making biological sense of a rapidly changing world. Clim. Change Responses 1, 6 (2014).
    Google Scholar 
    Pacifici, M. et al. Assessing species vulnerability to climate change. Nat. Clim. Change 5, 215 (2015).ADS 

    Google Scholar 
    Gunderson, A. R., Armstrong, E. J. & Stillman, J. H. Multiple stressors in a changing world: The need for an improved perspective on physiological responses to the dynamic marine environment. Annu. Rev. Mar. Sci. 8, 357–378 (2016).ADS 

    Google Scholar 
    Rilov, G. et al. Adaptive marine conservation planning in the face of climate change: What can we learn from physiological, ecological and genetic studies?. Glob. Ecol. Conserv. 17, e00566 (2019).
    Google Scholar 
    Hampe, A. Bioclimate envelope models: What they detect and what they hide. Glob. Ecol. Biogeogr. 13, 469–471 (2004).
    Google Scholar 
    Pearson, R. G. & Dawson, T. P. Predicting the impacts of climate change on the distribution of species: Are bioclimate envelope models useful?. Glob. Ecol. Biogeogr. 12, 361–371 (2003).
    Google Scholar 
    Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).PubMed 

    Google Scholar 
    Davis, A. J., Jenkinson, L. S., Lawton, J. H., Shorrocks, B. & Wood, S. Making mistakes when predicting shifts in species range in response to global warming. Nature 391, 783–786 (1998).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Araújo, M. B. & Peterson, A. T. Uses and misuses of bioclimatic envelope modeling. Ecology 93, 1527–1539 (2012).PubMed 

    Google Scholar 
    Helmuth, B. et al. Mosaic patterns of thermal stress in the rocky intertidal zone: Implications for climate change. Ecol. Monogr. 76, 461–479 (2006).
    Google Scholar 
    Helmuth, B., Mieszkowska, N., Moore, P. & Hawkins, S. J. Living on the edge of two changing worlds: Forecasting the responses of rocky intertidal ecosystems to climate change. Annu. Rev. Ecol. Evol. Syst. 37, 373–404 (2006).
    Google Scholar 
    Vasseur, D. A. et al. Synchronous dynamics of zooplankton competitors prevail in temperate lake ecosystems. Proc. R. Soc. B Biol. Sci. 281, 20140633 (2014).
    Google Scholar 
    Dillon, M. E. et al. Life in the frequency domain: The biological impacts of changes in climate variability at multiple time scales. Integr. Comp. Biol. icw024 (2016).Kroeker, K. J. et al. Interacting environmental mosaics drive geographic variation in mussel performance and predation vulnerability. Ecol. Lett. 19, 771–779 (2016).PubMed 

    Google Scholar 
    Seabra, R., Wethey, D. S., Santos, A. M. & Lima, F. P. Understanding complex biogeographic responses to climate change. Sci. Rep. 5, (2015).Di Cecco, G. J. & Gouhier, T. C. Increased spatial and temporal autocorrelation of temperature under climate change. Sci. Rep. 8, 14850 (2018).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Keppel, G. et al. Refugia: identifying and understanding safe havens for biodiversity under climate change. Glob. Ecol. Biogeogr. 21, 393–404 (2012).
    Google Scholar 
    Morelli, T. L. et al. Climate change refugia and habitat connectivity promote species persistence. Clim. Change Responses 4, 8 (2017).
    Google Scholar 
    Bates, A. E. et al. Biologists ignore ocean weather at their peril. Nature 560, 299–301 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Molinos, J. G. et al. Climate velocity and the future global redistribution of marine biodiversity. Nat. Clim. Change (2015).Levins, R. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomol. Soc. Am. 15, 237–240 (1969).
    Google Scholar 
    Brown, J. H. & Kodric-Brown, A. Turnover rates in insular biogeography: Effect of immigration on extinction. Ecology 58, 445–449 (1977).
    Google Scholar 
    Pulliam, H. R. Sources, sinks, and population regulation. Am. Nat. 132, 652–661 (1988).
    Google Scholar 
    Hannah, L. et al. Fine-grain modeling of species’ response to climate change: Holdouts, stepping-stones, and microrefugia. Trends Ecol. Evol. 29, 390–397 (2014).PubMed 

    Google Scholar 
    Barceló, C., Ciannelli, L. & Brodeur, R. D. Pelagic marine refugia and climatically sensitive areas in an eastern boundary current upwelling system. Glob. Change Biol. 24, 668–680 (2018).ADS 

    Google Scholar 
    Dong, Y. et al. Untangling the roles of microclimate, behaviour and physiological polymorphism in governing vulnerability of intertidal snails to heat stress. Proc. R. Soc. B Biol. Sci. 284, 20162367 (2017).
    Google Scholar 
    Smit, A. J. et al. A coastal seawater temperature dataset for biogeographical studies: large biases between in situ and remotely-sensed data sets around the Coast of South Africa. PLoS ONE 8, e81944 (2013).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Castro, S. L., Monzon, L. A., Wick, G. A., Lewis, R. D. & Beylkin, G. Subpixel variability and quality assessment of satellite sea surface temperature data using a novel High Resolution Multistage Spectral Interpolation (HRMSI) technique. Remote Sens. Environ. 217, 292–308 (2018).ADS 

    Google Scholar 
    Rahaghi, A. I., Lemmin, U. & Barry, D. A. Surface water temperature heterogeneity at subpixel satellite scales and its effect on the surface cooling estimates of a large lake: Airborne remote sensing results from Lake Geneva. J. Geophys. Res. Oceans 124, 635–651 (2019).ADS 

    Google Scholar 
    Pfister, C. A., Wootton, J. T. & Neufeld, C. J. The relative roles of coastal and oceanic processes in determining physical and chemical characteristics of an intensively sampled nearshore system. Limnol. Oceanogr. 52, 1767–1775 (2007).ADS 
    CAS 

    Google Scholar 
    Meneghesso, C. et al. Remotely-sensed L4 SST underestimates the thermal fingerprint of coastal upwelling. Remote Sens. Environ. 237, 111588 (2020).ADS 

    Google Scholar 
    Leichter, J. J., Helmuth, B. & Fischer, A. M. Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida. J. Mar. Res. 64, 563–588 (2006).
    Google Scholar 
    Castillo, K. D. & Lima, F. P. Comparison of in situ and satellite-derived (MODIS-Aqua/Terra) methods for assessing temperatures on coral reefs. Limnol. Oceanogr. Methods 8, 107–117 (2010).
    Google Scholar 
    Wyatt, A. S. J. et al. Heat accumulation on coral reefs mitigated by internal waves. Nat. Geosci. 13, 28–34 (2020).ADS 
    CAS 

    Google Scholar 
    Lourenço, C. R. et al. Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. J. Biogeogr. 43, 1595–1607 (2016).
    Google Scholar 
    Seabra, R. et al. Reduced nearshore warming associated with eastern boundary upwelling systems. Front. Mar. Sci. 6, (2019).Randall, C. J., Toth, L. T., Leichter, J. J., Maté, J. L. & Aronson, R. B. Upwelling buffers climate change impacts on coral reefs of the eastern tropical Pacific. Ecology 101, (2020).Varela, R., Lima, F. P., Seabra, R., Meneghesso, C. & Gómez-Gesteira, M. Coastal warming and wind-driven upwelling: A global analysis. Sci. Total Environ. 639, 1501–1511 (2018).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Schulz, K. G., Hartley, S. & Eyre, B. Upwelling amplifies ocean acidification on the east Australian shelf: Implications for marine ecosystems. Front. Mar. Sci. 6, (2019).Connell, J. H. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42, 710–723 (1961).
    Google Scholar 
    Somero, G. N. Linking biogeography to physiology: Evolutionary and acclimatory adjustments of thermal limits. Front. Zool. 2, 1 (2005).PubMed 
    PubMed Central 

    Google Scholar 
    Sydeman, W. J. et al. Climate change and wind intensification in coastal upwelling ecosystems. Science 345, 77–80 (2014).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Sweijd, N. A. & Smit, A. J. Trends in sea surface temperature and chlorophyll-a in the seven African Large Marine Ecosystems. Environ. Dev. 36, 100585 (2020).
    Google Scholar 
    Wang, D., Gouhier, T. C., Menge, B. A. & Ganguly, A. R. Intensification and spatial homogenization of coastal upwelling under climate change. Nature 518, 390–394 (2015).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Lima, F. P. & Wethey, D. S. Robolimpets: measuring intertidal body temperatures using biomimetic loggers: Biomimetic loggers for intertidal temperatures. Limnol. Oceanogr. Methods 7, 347–353 (2009).
    Google Scholar 
    Judge, R., Choi, F. & Helmuth, B. Recent advances in data logging for intertidal ecology. Front. Ecol. Evol. 6, (2018).Harley, C. D. G. & Helmuth, B. S. T. Local- and regional-scale effects of wave exposure, thermal stress, and absolute versus effective shore level on patterns of intertidal zonation. Limnol. Oceanogr. 48, 1498–1508 (2003).ADS 

    Google Scholar 
    Seabra, R., Wethey, D. S., Santos, A. M., Gomes, F. & Lima, F. P. Equatorial range limits of an intertidal ectotherm are more linked to water than air temperature. Glob. Change Biol. 22, 3320–3331 (2016).ADS 

    Google Scholar 
    Lima, F. P. et al. Loss of thermal refugia near equatorial range limits. Glob. Change Biol. 22, 254–263 (2016).ADS 

    Google Scholar 
    Tapia, F. J. et al. Thermal indices of upwelling effects on inner-shelf habitats. Prog. Oceanogr. 83, 278–287 (2009).ADS 

    Google Scholar 
    Freeman, E. et al. ICOADS release 3.0: A major update to the historical marine climate record. Int. J. Climatol. 37, 2211–2232 (2017).
    Google Scholar 
    Lemos, R. T. & Pires, H. O. The upwelling regime off the West Portuguese Coast, 1941–2000. Int. J. Climatol. 24, 511–524 (2004).
    Google Scholar 
    Seabra, R., Wethey, D. S., Santos, A. M. & Lima, F. P. Side matters: Microhabitat influence on intertidal heat stress over a large geographical scale. J. Exp. Mar. Biol. Ecol. 400, 200–208 (2011).
    Google Scholar 
    Legendre, P. Species associations: The Kendall coefficient of concordance revisited. J. Agric. Biol. Environ. Stat. 10, 226–245 (2005).
    Google Scholar 
    Gouhier, T. C. & Guichard, F. Synchrony: Quantifying variability in space and time. Methods Ecol. Evol. 5, 524–533 (2014).
    Google Scholar 
    Torrence, C. & Compo, G. P. A practical guide to wavelet analysis. Bull. Am. Meteorol. Soc. 79, 61–78 (1998).ADS 

    Google Scholar 
    Cazelles, B. et al. Wavelet analysis of ecological time series. Oecologia 156, 287–304 (2008).ADS 
    PubMed 

    Google Scholar 
    Recknagel, F., Ostrovsky, I., Cao, H., Zohary, T. & Zhang, X. Ecological relationships, thresholds and time-lags determining phytoplankton community dynamics of Lake Kinneret, Israel elucidated by evolutionary computation and wavelets. Ecol. Model. 255, 70–86 (2013).CAS 

    Google Scholar 
    Mislan, K. A. S., Helmuth, B. & Wethey, D. S. Geographical variation in climatic sensitivity of intertidal mussel zonation: Biogeography of climatic sensitivity. Glob. Ecol. Biogeogr. 23, 744–756 (2014).
    Google Scholar 
    Grinsted, A., Moore, J. C. & Jevrejeva, S. Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Process. Geophys. 11, 561–566 (2004).ADS 

    Google Scholar 
    Cazelles, B. & Stone, L. Detection of imperfect population synchrony in an uncertain world. J. Anim. Ecol. 72, 953–968 (2003).
    Google Scholar 
    Keppel, G. et al. The capacity of refugia for conservation planning under climate change. Front. Ecol. Environ. 13, 106–112 (2015).
    Google Scholar 
    Vasseur, D. A. et al. Increased temperature variation poses a greater risk to species than climate warming. Proc. R. Soc. B Biol. Sci. 281, 20132612–20132612 (2014).
    Google Scholar 
    Potter, K. A., Woods, H. A. & Pincebourde, S. Microclimatic challenges in global change biology. Glob. Change Biol. 19, 2932–2939 (2013).ADS 

    Google Scholar 
    Sandel, B. et al. The influence of late quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Pinsky, M. L., Worm, B., Fogarty, M. J., Sarmiento, J. L. & Levin, S. A. Marine taxa track local climate velocities. Science 341, 1239–1242 (2013).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Araújo, M. B. & Luoto, M. The importance of biotic interactions for modelling species distributions under climate change. Glob. Ecol. Biogeogr. 16, 743–753 (2007).
    Google Scholar 
    Morelli, T. L. et al. Managing climate change refugia for climate adaptation. PLoS ONE 11, e0159909 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Stenseth, N. Ecological effects of climate fluctuations. Science 297, 1292–1296 (2002).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Zellweger, F., De Frenne, P., Lenoir, J., Rocchini, D. & Coomes, D. Advances in microclimate ecology arising from remote sensing. Trends Ecol. Evol. 34, 327–341 (2019).PubMed 

    Google Scholar 
    Helmuth, B. et al. Long-term, high frequency in situ measurements of intertidal mussel bed temperatures using biomimetic sensors. Sci. Data 3, 160087 (2016).MathSciNet 
    PubMed 
    PubMed Central 

    Google Scholar 
    Wikelski, M. & Cooke, S. J. Conservation physiology. Trends Ecol. Evol. 21, 38–46 (2006).PubMed 

    Google Scholar 
    Helmuth, B. S. T. & Hofmann, G. E. Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biol. Bull. 201, 374–384 (2001).CAS 
    PubMed 

    Google Scholar 
    Kearney, M. Habitat, environment and niche: What are we modelling?. Oikos 115, 186–191 (2006).
    Google Scholar 
    Ashcroft, M. B. Identifying refugia from climate change. J. Biogeogr. 37, 1407–1413 (2010).
    Google Scholar 
    Maggs, C. A. et al. Evaluating signatures of glacial refugia for North Atlantic Benthic Marine Taxa. Ecology 89, S108–S122 (2008).PubMed 

    Google Scholar 
    Bennett, K. & Provan, J. What do we mean by ‘refugia’?. Quat. Sci. Rev. 27, 2449–2455 (2008).ADS 

    Google Scholar 
    Ashcroft, M. B., Chisholm, L. A. & French, K. O. Climate change at the landscape scale: predicting fine-grained spatial heterogeneity in warming and potential refugia for vegetation. Glob. Change Biol. 15, 656–667 (2009).ADS 

    Google Scholar 
    Hofmann, G. E. et al. High-frequency dynamics of ocean pH: A multi-ecosystem comparison. PLoS ONE 6, e28983 (2011).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bakun, A. et al. Anticipated Effects of Climate Change on Coastal Upwelling Ecosystems. Curr. Clim. Change Rep. 1, 85–93 (2015).
    Google Scholar 
    Iles, A. C. et al. Climate-driven trends and ecological implications of event-scale upwelling in the California Current System. Glob. Change Biol. 18, 783–796 (2012).ADS 

    Google Scholar 
    García-Reyes, M. et al. Under pressure: Climate change, upwelling, and eastern boundary upwelling ecosystems. Front. Mar. Sci. 2, (2015).Liebhold, A., Koenig, W. D. & Bjørnstad, O. N. Spatial synchrony in population dynamics. Annu. Rev. Ecol. Evol. Syst. 467–490 (2004).Amarasekare, P. & Nisbet, R. M. Spatial heterogeneity, source-sink dynamics, and the local coexistence of competing species. Am. Nat. 158, 572–584 (2001).CAS 
    PubMed 

    Google Scholar 
    Adler, F. R. & Nuernberger, B. Persistence in patchy irregular landscapes. Theor. Popul. Biol. 45, 41–75 (1994).MATH 

    Google Scholar 
    Rykaczewski, R. R. et al. Poleward displacement of coastal upwelling-favorable winds in the ocean’s eastern boundary currents through the 21st century. Geophys. Res. Lett. 42, 6424–6431 (2015).ADS 

    Google Scholar 
    Varela, R., Rodríguez-Díaz, L., de Castro, M. & Gómez-Gesteira, M. Influence of Canary upwelling system on coastal SST warming along the 21st century using CMIP6 GCMs. Glob. Planet. Change 208, 103692 (2022).
    Google Scholar 
    Ocean deoxygenation: everyone’s problem. Causes, impacts, consequences and solutions. (IUCN, International Union for Conservation of Nature, 2019). https://doi.org/10.2305/IUCN.CH.2019.13.en.Howard, E. M. et al. Climate-driven aerobic habitat loss in the California Current System. Sci. Adv. 6, eaay3188 (2020).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Iles, A. C. Toward predicting community-level effects of climate: Relative temperature scaling of metabolic and ingestion rates. Ecology 95, 2657–2668 (2014).
    Google Scholar 
    Harris, R. M. B. et al. Biological responses to the press and pulse of climate trends and extreme events. Nat. Clim. Change 8, 579 (2018).ADS 

    Google Scholar 
    Salinas, S., Irvine, S. E., Schertzing, C. L., Golden, S. Q. & Munch, S. B. Trait variation in extreme thermal environments under constant and fluctuating temperatures. Philos. Trans. R. Soc. B Biol. Sci. 374, 20180177 (2019).
    Google Scholar 
    Fischer, E. M. & Knutti, R. Anthropogenic contribution to global occurrence of heavy-precipitation and high-temperature extremes. Nat. Clim. Change 5, 560–564 (2015).ADS 

    Google Scholar 
    Buckley, L. B. & Huey, R. B. Temperature extremes: geographic patterns, recent changes, and implications for organismal vulnerabilities. Glob. Change Biol. 22, 3829–3842 (2016).ADS 

    Google Scholar  More

  • in

    Mixtures of genotypes increase disease resistance in a coral nursery

    Vega Thurber, R. et al. Deciphering coral disease dynamics: Integrating host, microbiome, and the changing environment. Front. Ecol. Evol. 2020, 8 (2020).
    Google Scholar 
    Groner, M. L. et al. Managing marine disease emergencies in an era of rapid change. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371, 1689 (2016).
    Google Scholar 
    Richardson, L. L. Coral diseases: What is really known?. Trends Ecol. Evol. 13, 438–443 (1998).CAS 
    PubMed 

    Google Scholar 
    Miller, M. W., Lohr, K. E., Cameron, C. M., Williams, D. E. & Peters, E. C. Disease dynamics and potential mitigation among restored and wild staghorn coral, Acropora cervicornis. PeerJ https://doi.org/10.7287/peerj.preprints.328 (2014).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Teplitski, M. & Ritchie, K. How feasible is the biological control of coral diseases?. Trends Ecol. Evol. 24, 378–385 (2009).PubMed 

    Google Scholar 
    Zhu, Y. et al. Genetic diversity and disease control in rice. Nature 406, 718–722 (2000).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Altermatt, F. & Ebert, D. Genetic diversity of Daphnia magna populations enhances resistance to parasites. Ecol. Lett. 11, 918–928 (2008).PubMed 

    Google Scholar 
    Aronson, R. B. & Precht, W. F. White-band disease and the changing face of Caribbean coral reefs. In (ed Porter, J. W.) The Ecology and Etiology of Newly Emerging Marine Diseases 25–38 (Springer Netherlands, 2001).Ruiz-Moreno, D. et al. Global coral disease prevalence associated with sea temperature anomalies and local factors. Dis. Aquat. Organ. 100, 249–261 (2012).PubMed 

    Google Scholar 
    Precht, W. F., Gintert, B. E., Robbart, M. L., Fura, R. & van Woesik, R. Unprecedented disease-related coral mortality in Southeastern Florida. Sci. Rep. 6, 31374 (2016).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Gignoux-Wolfsohn, S. A., Marks, C. J. & Vollmer, S. V. White Band Disease transmission in the threatened coral, Acropora cervicornis. Sci. Rep. 2, 804 (2012).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Aronson, R., Bruckner, A., Moore, J., Precht, B. & Weil, E. Acropora cervicornis. IUCN Red List of Threatened Species https://doi.org/10.2305/iucn.uk.2008.rlts.t133381a3716457.en (2008).Alvarez-Filip, L., González-Barrios, F. J., Pérez-Cervantes, E., Molina-Hernández, A. & Estrada-Saldívar, N. Stony coral tissue loss disease decimated Caribbean coral populations and reshaped reef functionality. Commun. Biol. 5, 440 (2022).PubMed 
    PubMed Central 

    Google Scholar 
    Heres, M. M., Farmer, B. H., Elmer, F. & Hertler, H. Ecological consequences of Stony Coral Tissue Loss Disease in the Turks and Caicos Islands. Coral Reefs 40, 609–624 (2021).
    Google Scholar 
    Neely, K. L., Shea, C. P., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Short- and long-term effectiveness of coral disease treatments. Front. Mar. Sci. 2021, 8 (2021).
    Google Scholar 
    Neely, K. L., Macaulay, K. A., Hower, E. K. & Dobler, M. A. Effectiveness of topical antibiotics in treating corals affected by stony coral tissue loss disease. PeerJ 8, e9289 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Shilling, E. N., Combs, I. R. & Voss, J. D. Assessing the effectiveness of two intervention methods for stony coral tissue loss disease on Montastraea cavernosa. Sci. Rep. 11, 8566 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Walker, B. K., Turner, N. R., Noren, H. K. G., Buckley, S. F. & Pitts, K. A. Optimizing stony coral tissue loss disease (SCTLD) intervention treatments on Montastraea cavernosa in an Endemic Zone. Front. Mar. Sci. 8, 666224 (2021).
    Google Scholar 
    Forrester, G. E., Arton, L., Horton, A., Nickles, K. & Forrester, L. M. Antibiotic treatment ameliorates the impact of stony coral tissue loss disease (SCTLD) on coral communities. Front. Mar. Sci. 2022, 9 (2022).
    Google Scholar 
    Lee-Hing, C. et al. Management responses in Belize and Honduras, as stony coral tissue loss disease expands its prevalence in the Mesoamerican reef. Front. Mar. Sci. 9, 1 (2022).ADS 

    Google Scholar 
    Young, C. N., Schopmeyer, S. A. & Lirman, D. A review of reef restoration and coral propagation using the threatened genus Acropora in the Caribbean and Western Atlantic. Bull. Mar. Sci. 88, 1075–1098 (2012).
    Google Scholar 
    Lirman, D. & Schopmeyer, S. Ecological solutions to reef degradation: Optimizing coral reef restoration in the Caribbean and Western Atlantic. PeerJ 4, e2597 (2016).PubMed 
    PubMed Central 

    Google Scholar 
    Baums, I. B. et al. Considerations for maximizing the adaptive potential of restored coral populations in the western Atlantic. Ecol. Appl. 29, e01978 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Rosales, S. M. et al. Microbiome differences in disease-resistant vs susceptible Acropora corals subjected to disease challenge assays. Sci. Rep. 9, 18279 (2019).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Pinzón, C. J. H., Beach-Letendre, J., Weil, E. & Mydlarz, L. D. Relationship between phylogeny and immunity suggests older caribbean coral lineages are more resistant to disease. PLoS ONE 9, e104787. https://doi.org/10.1371/journal.pone.0104787 (2014).Article 
    ADS 
    CAS 

    Google Scholar 
    Drury, C. et al. Genomic patterns in Acropora cervicornis show extensive population structure and variable genetic diversity. Ecol. Evol. 7, 6188–6200 (2017).PubMed 
    PubMed Central 

    Google Scholar 
    Maneval, P., Jacoby, C. A., Harris, H. E. & Frazer, T. K. Genotype, nursery design, and depth influence the growth of Acropora cervicornis fragments. Front. Mar. Sci. 8, 1 (2021).
    Google Scholar 
    Wright, R. M. et al. Intraspecific differences in molecular stress responses and coral pathobiome contribute to mortality under bacterial challenge in Acropora millepora. Sci. Rep. 7, 2609 (2017).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Vollmer, S. V. & Kline, D. I. Natural disease resistance in threatened staghorn corals. PLoS ONE 3, e3718 (2008).ADS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, N., Maneval, P., Manfrino, C., Frazer, T. K. & Meyer, J. L. Spatial distribution of microbial communities among colonies and genotypes in nursery-reared Acropora cervicornis. PeerJ 8, e9635 (2020).PubMed 
    PubMed Central 

    Google Scholar 
    Klinges, G., Maher, R. L., Vega-Thurber, R. L. & Muller, E. M. Parasitic, “Candidatus Aquarickettsia rohweri” is a marker of disease susceptibility in Acropora cervicornis but is lost during thermal stress. Environ. Microbiol. 22, 5341–5355 (2020).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Miller, M. W. et al. Genotypic variation in disease susceptibility among cultured stocks of elkhorn and staghorn corals. PeerJ 7, e6751 (2019).PubMed 
    PubMed Central 

    Google Scholar 
    Rohr, J. R. et al. Towards common ground in the biodiversity-disease debate. Nat. Ecol. Evol. 4, 24–33 (2020).PubMed 

    Google Scholar 
    Shearer, T. L., Porto, I. & Zubillaga, A. L. Restoration of coral populations in light of genetic diversity estimates. Coral Reefs 28, 727–733 (2009).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Ostfeld, R. S. & Keesing, F. Biodiversity and disease risk: The case of lyme disease. Conserv. Biol. 14, 722–728 (2000).
    Google Scholar 
    Lively, C. M. The effect of host genetic diversity on disease spread. Am. Nat. 175, E149–E152 (2010).PubMed 

    Google Scholar 
    Ostfeld, R. S. & Keesing, F. Effects of host diversity on infectious disease. Annu. Rev. Ecol. Evol. Syst. 43, 157–182 (2012).
    Google Scholar 
    King, K. C. & Lively, C. M. Does genetic diversity limit disease spread in natural host populations?. Heredity 109, 199–203 (2012).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Acevedo-Whitehouse, K., Gulland, F., Greig, D. & Amos, W. Inbreeding: Disease susceptibility in California sea lions. Nature 422, 35 (2003).ADS 
    CAS 
    PubMed 

    Google Scholar 
    O’Brien, S. J. et al. Genetic basis for species vulnerability in the cheetah. Science 227, 1428–1434 (1985).ADS 
    PubMed 

    Google Scholar 
    Pearman, P. B. & Garner, T. W. J. Susceptibility of Italian agile frog populations to an emerging strain of Ranavirus parallels population genetic diversity. Ecol. Lett. 8, 401–408 (2005).
    Google Scholar 
    Reber, A., Castella, G., Christe, P. & Chapuisat, M. Experimentally increased group diversity improves disease resistance in an ant species. Ecol. Lett. 11, 682–689 (2008).PubMed 

    Google Scholar 
    Mundt, C. C. Use of multiline cultivars and cultivar mixtures for disease management. Annu. Rev. Phytopathol. 40, 381–410 (2002).CAS 
    PubMed 

    Google Scholar 
    Elton, C. S. The Ecology of Invasions by Animals and Plants (University of Chicago Press, 2000).
    Google Scholar 
    Schopmeyer, S. A. et al. Regional restoration benchmarks for Acropora cervicornis. Coral Reefs 36, 1047–1057 (2017).ADS 

    Google Scholar 
    Baums, I. B., Miller, M. W. & Hellberg, M. E. Geographic variation in clonal structure in a reef-building Caribbean coral, Acropora palmata. Ecol. Monogr. 76, 503–519 (2006).
    Google Scholar 
    Gignoux-Wolfsohn, S. A., Precht, W. F., Peters, E. C., Gintert, B. E. & Kaufman, L. S. Ecology, histopathology, and microbial ecology of a white-band disease outbreak in the threatened staghorn coral Acropora cervicornis. Dis. Aquat. Organ. 137, 217–237 (2020).PubMed 

    Google Scholar 
    Gignoux-Wolfsohn, S. A. & Vollmer, S. V. Identification of candidate coral pathogens on white band disease-infected staghorn coral. PLoS ONE 10, e0134416 (2015).PubMed 
    PubMed Central 

    Google Scholar 
    Brooks, M. et al. GlmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J. 9, 378–400 (2017).
    Google Scholar 
    Fox, J. & Weisburg, S. An R Companion to Applied Regression 3rd edn. (Sage, 2019).
    Google Scholar  More

  • in

    Temporal and functional interrelationships between bacterioplankton communities and the development of a toxigenic Microcystis bloom in a lowland European reservoir

    Paerl, H. W. Mitigating toxic planktonic cyanobacterial blooms in aquatic ecosystems facing increasing anthropogenic and climatic pressures. Toxins. 10, 1–16 (2018).
    Google Scholar 
    Harke, M. J. et al. A review of the global ecology, genomics, and biogeography of the toxic cyanobacterium Microcystis spp. Harmful Algae 54, 4–20. https://doi.org/10.1016/j.hal.2015.12.007 (2016).Article 
    PubMed 

    Google Scholar 
    Paerl, H. W. & Barnard, M. A. Mitigating the global expansion of harmful cyanobacterial blooms: Moving targets in a human- and climatically-altered world. Harmful Algae 96, 101845. https://doi.org/10.1016/j.hal.2020.101845 (2020).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Paerl, H. W. Mitigating harmful cyanobacterial blooms in a human- and climatically-impacted world. Life. 4, 988–1012 (2014).PubMed 
    PubMed Central 

    Google Scholar 
    Burford, M. A. et al. Perspective: Advancing the research agenda for improving understanding of cyanobacteria in a future of global change. Harmful Algae 91, 101601. https://doi.org/10.1016/j.hal.2019.04.004 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Havens, K. E., James, R. T., East, T. L. & Smith, V. H. N: P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environ. Pollut. 122, 379–390 (2003).CAS 
    PubMed 

    Google Scholar 
    Bernard, C. Cyanobacteria and cyanotoxins. Rev. Franç. Lab. 2014, 53–68 (2014).
    Google Scholar 
    Paerl, H. W. & Otten, T. G. Harmful cyanobacterial blooms: Causes, consequences, and controls. Microb. Ecol. 65, 995–1010 (2013).CAS 
    PubMed 

    Google Scholar 
    Dolman, A. M. et al. Cyanobacteria and cyanotoxins: The influence of nitrogen versus phosphorus. PLoS ONE 7, 38575 (2012).
    Google Scholar 
    Svirčev, Z. et al. Global geographical and historical overview of cyanotoxin distribution and cyanobacterial poisonings. Arch. Toxicol. https://doi.org/10.1007/s00204-019-02524-4 (2019).Article 
    PubMed 

    Google Scholar 
    Massey, I. Y. & Yang, F. A mini review on microcystins and bacterial degradation. Toxins 12, 268 (2020).CAS 
    PubMed Central 

    Google Scholar 
    Paerl, H. W. et al. Mitigating eutrophication and toxic cyanobacterial blooms in large lakes: The evolution of a dual nutrient (N and P) reduction paradigm. Hydrobiologia 847, 4359–4375. https://doi.org/10.1007/s10750-019-04087-y (2020).Article 
    CAS 

    Google Scholar 
    Sapp, M. et al. Species-specific bacterial communities in the phycosphere of microalgae?. Microb. Ecol. 53, 683–699 (2007).PubMed 

    Google Scholar 
    Cai, H., Jiang, H., Krumholz, L. R. & Yang, Z. Bacterial community composition of size-fractioned aggregates within the phycosphere of cyanobacterial blooms in a eutrophic freshwater lake. PLoS ONE 9, 102879 (2014).ADS 

    Google Scholar 
    Grant, M. A. A., Kazamia, E., Cicuta, P. & Smith, A. G. Direct exchange of vitamin B 12 is demonstrated by modelling the growth dynamics of algal-bacterial cocultures. ISME J. Nat. Publ. Group 8, 1418–1427 (2014).CAS 

    Google Scholar 
    Shi, L., Cai, Y., Kong, F. & Yu, Y. Specific association between bacteria and buoyant Microcystis colonies compared with other bulk bacterial communities in the eutrophic Lake Taihu, China. Environ. Microbiol. Rep. 4, 669–678 (2012).CAS 
    PubMed 

    Google Scholar 
    Brunberg, A. K. Contribution of bacteria in the mucilage of Microcystis spp (Cyanobacteria) to benthic and pelagic bacterial production in a hypereutrophic lake. FEMS Microbiol. Ecol. 29, 13–22 (1999).CAS 

    Google Scholar 
    Shao, K. et al. The responses of the taxa composition of particle-attached bacterial community to the decomposition of Microcystis blooms. Sci. Total. Environ. 488–489, 236–242. https://doi.org/10.1016/j.scitotenv.2014.04.101 (2014).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Jankowiak, J. G. & Gobler, C. J. The composition and function of microbiomes within microcystis colonies are significantly different than native bacterial assemblages in two North American lakes. Front. Microbiol. 11, 1–26 (2020).
    Google Scholar 
    Bauer, A. & Forchhammer, K. Bacterial predation on cyanobacteria. Microb. Physiol. 99, 108 (2021).
    Google Scholar 
    Ndlela, L. L., Oberholster, P. J., Van Wyk, J. H. & Cheng, P. H. Bacteria as biological control agents of freshwater cyanobacteria: Is it feasible beyond the laboratory?. Appl. Microbiol. Biotechnol. 102, 9911–9923 (2018).CAS 
    PubMed 

    Google Scholar 
    Yang, C. et al. Distinct network interactions in particle-associated and free-living bacterial communities during a Microcystis aeruginosa bloom in a plateau lake. Front. Microbiol. 8, 1–15 (2017).
    Google Scholar 
    Xu, H. et al. Contrasting network features between free-living and particle-attached bacterial communities in Taihu Lake. Microb. Ecol. 76, 303–313 (2018).PubMed 

    Google Scholar 
    Liu, M. et al. Community dynamics of free-living and particle-attached bacteria following a reservoir Microcystis bloom. Sci. Total Environ. 660, 501–511. https://doi.org/10.1016/j.scitotenv.2018.12.414 (2019).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Parveen, B. et al. Bacterial communities associated with Microcystis colonies differ from free-living communities living in the same ecosystem. Environ. Microbiol. Rep. 5, 716–724 (2013).CAS 
    PubMed 

    Google Scholar 
    Louati, I. et al. Structural diversity of bacterial communities associated with bloom-forming freshwater cyanobacteria differs according to the cyanobacterial genus. PLoS ONE 10, 0140614 (2015).
    Google Scholar 
    Zwirglmaier, K., Keiz, K., Engel, M., Geist, J. & Raeder, U. Seasonal and spatial patterns of microbial diversity along a trophic gradient in the interconnected lakes of the Osterseen Lake District, Bavaria. Front. Microbiol. 6, 1–18 (2015).
    Google Scholar 
    Scherer, P. I. et al. Temporal dynamics of the microbial community composition with a focus on toxic cyanobacteria and toxin presence during harmful algal blooms in two South German lakes. Front. Microbiol. 8, 1–17 (2017).
    Google Scholar 
    Kokocinski, M., Dziga, D., Antosiak, A. & Soininen, J. Are bacterio- and phytoplankton community compositions related in lakes differing in their cyanobacteria contribution and physico-chemical properties?. Genes 12, 855 (2021).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dziga, D. et al. Correlation between specific groups of heterotrophic bacteria and microcystin biodegradation in freshwater bodies of central Europe. FEMS Microbiol. Ecol. https://doi.org/10.1111/j.1574-6941.1999.tb00594.x (2019).Article 
    PubMed 

    Google Scholar 
    Jurczak, T. et al. Elimination of microcystins by water treatment processes: Examples from Sulejow Reservoir, Poland. Water Res. 39, 2394–2406 (2005).CAS 
    PubMed 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Detection and monitoring toxigenicity of cyanobacteria by application of molecular methods. Environ Toxicol. 21, 380–387 (2006).ADS 
    CAS 
    PubMed 

    Google Scholar 
    Rajaniemi-Wacklin, P. et al. Correspondence between phylogeny and morphology of Snowella spp. and Woronichinia naegeliana, cyanobacteria commonly occurring in lakes. J. Phycol. 42, 226–232 (2006).
    Google Scholar 
    DrobacBacković, D. et al. Cyanobacteria, cyanotoxins, and their histopathological effects on fish tissues in Fehérvárcsurgó reservoir Hungary. Environ. Monit. Assess. https://doi.org/10.1007/s10661-021-09324-3 (2021).Article 

    Google Scholar 
    Kallscheuer, N. et al. Analysis of bacterial communities in a municipal duck pond during a phytoplankton bloom and isolation of Anatilimnocola aggregata gen. nov., sp. Nov., Lacipirellula limnantheis sp. Nov. and Urbifossiella limnaea gen. nov. sp. nov. belonging to the phylum. Environ. Microbiol. 23, 1379–1396 (2021).CAS 
    PubMed 

    Google Scholar 
    Davis, T. W. et al. Effects of nitrogenous compounds and phosphorus on the growth of toxic and non-toxic strains of Microcystis during cyanobacterial blooms. Aquat. Microb. Ecol. 61, 149–162 (2010).
    Google Scholar 
    Gobler, C. J., Davis, T. W., Coyne, K. J. & Boyer, G. L. Interactive influences of nutrient loading, zooplankton grazing, and microcystin synthetase gene expression on cyanobacterial bloom dynamics in a eutrophic New York lake. Harmful Algae 6, 119–133 (2007).CAS 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Cyanophages infection of microcystis bloom in lowland dam reservoir of Sulejów, Poland. Microb. Ecol. 71, 315–325 (2016).CAS 
    PubMed 

    Google Scholar 
    Davis, T. W., Berry, D. L., Boyer, G. L. & Gobler, C. J. The effects of temperature and nutrients on the growth and dynamics of toxic and non-toxic strains of Microcystis during cyanobacteria blooms. Harmful Algae 8, 715–725 (2009).CAS 

    Google Scholar 
    Yoshida, M., Yoshida, T., Takashima, Y., Hosoda, N. & Hiroishi, S. Dynamics of microcystin-producing and non-microcystin-producing Microcystis populations is correlated with nitrate concentration in a Japanese lake. FEMS Microbiol. Lett. 266, 49–53 (2007).CAS 
    PubMed 

    Google Scholar 
    Sezenna, M. L. Proteobacteria: Phylogeny, Metabolic Diversity and Ecological Effects (Nova Science Publishers, Inc., 2011).
    Google Scholar 
    Rilling, J. I., Acuña, J. J., Sadowsky, M. J. & Jorquera, M. A. Putative nitrogen-fixing bacteria associated with the rhizosphere and root endosphere of wheat plants grown in an andisol from southern Chile. Front. Microbiol. 9, 1–13 (2018).
    Google Scholar 
    Lukumbuzya, M. et al. A refined set of rRNA-targeted oligonucleotide probes for in situ detection and quantification of ammonia-oxidizing bacteria. Water Res. 186, 116375 (2020).
    Google Scholar 
    Prosser, J. I., Head, I. M. & Stein, L. Y. The family Nitrosomonadaceae. In The Prokaryotes: Alphaproteobacteria and Betaproteobacteria (eds Rosenberg, E. et al.) 901–918 (Springer, 2014). https://doi.org/10.1007/978-3-642-30197-1_372.Chapter 

    Google Scholar 
    Jia, L., Jiang, B., Huang, F. & Hu, X. Nitrogen removal mechanism and microbial community changes of bioaugmentation subsurface wastewater infiltration system. Bioresour. Technol. 294, 122140. https://doi.org/10.1016/j.biortech.2019.122140 (2019).Article 
    CAS 
    PubMed 

    Google Scholar 
    Daft, M. J. & Stewart, W. D. P. Bacterial pathogens of freshwater blue-green algae. New Phytol. 70, 819–829 (1971).
    Google Scholar 
    Chun, S. J. et al. Network analysis reveals succession of Microcystis genotypes accompanying distinctive microbial modules with recurrent patterns. Water Res. 170, 115326. https://doi.org/10.1016/j.watres.2019.115326 (2020).Article 
    CAS 
    PubMed 

    Google Scholar 
    Parulekar, N. N. et al. Characterization of bacterial community associated with phytoplankton bloom in a eutrophic lake in South Norway using 16S rRNA gene amplicon sequence analysis. PLoS ONE 12, 1–22 (2017).
    Google Scholar 
    Guedes, I. A. et al. Close link between harmful cyanobacterial dominance and associated bacterioplankton in a tropical eutrophic reservoir. Front. Microbiol. 9, 424 (2018).PubMed 
    PubMed Central 

    Google Scholar 
    Allgaier, M. & Grossart, H. P. Seasonal dynamics and phylogenetic diversity of free-living and particle-associated bacterial communities in four lakes in northeastern Germany. Aquat. Microb. Ecol. 45, 115–128 (2006).
    Google Scholar 
    Chen, S. et al. Disentangling the drivers of Microcystis decomposition: Metabolic profile and co-occurrence of bacterial community. Sci. Total Environ. 739, 140062. https://doi.org/10.1016/j.scitotenv.2020.140062 (2020).Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar 
    Leflaive, J. & Ten-Hage, L. Algal and cyanobacterial secondary metabolites in freshwaters: A comparison of allelopathic compounds and toxins. Freshw. Biol. 52, 199–214 (2007).CAS 

    Google Scholar 
    Song, H. et al. Biological and chemical factors driving the temporal distribution of cyanobacteria and heterotrophic bacteria in a eutrophic lake (West Lake, China). Appl. Microbiol. Biotechnol. 101, 1685–1696. https://doi.org/10.1007/s00253-016-7968-8 (2017).Article 
    CAS 
    PubMed 

    Google Scholar 
    Bagatini, I. L. et al. Host-specificity and dynamics in bacterial communities associated with bloom-forming freshwater phytoplankton. PLoS ONE 9, 85957 (2014).ADS 

    Google Scholar 
    Kohler, E. et al. Biodegradation of microcystins during gravity-driven membrane (GDM) ultrafiltration. PLoS ONE 9, 111794 (2014).ADS 

    Google Scholar 
    Wu, X. et al. Culturing of “unculturable” subsurface microbes: Natural organic carbon source fuels the growth of diverse and distinct bacteria from groundwater. Front. Microbiol. 11, 1–10 (2020).CAS 

    Google Scholar 
    Morotomi, M., Nagai, F. & Watanabe, Y. Parasutterella secunda sp. no., isolated from human faeces and proposal of Sutterellaceae fam. nov. in the order Burkholderiales. Int. J. Syst. Evol. Microbiol. 61, 637–643 (2011).CAS 
    PubMed 

    Google Scholar 
    Kiedrzyńska, E. et al. Point sources of nutrient pollution in the lowland river catchment in the context of the baltic Sea eutrophication. Ecol. Eng. 70, 337–348 (2014).
    Google Scholar 
    Hwang, W. M., Ko, Y., Kim, J. H. & Kang, K. Ahniella affigens gen Nov, sp. nov., a gammaproteobacterium isolated from sandy soil near a stream. Int. J. Syst. Evol. Microbiol. 68, 2478–2484 (2018).CAS 
    PubMed 

    Google Scholar 
    Qian, H. et al. Spatial variability of cyanobacteria and heterotrophic bacteria in Lake Taihu (China). Bull. Environ. Contam. Toxicol. 99, 380–384 (2017).CAS 
    PubMed 

    Google Scholar 
    Humbert, J. F. et al. Comparison of the structure and composition of bacterial communities from temperate and tropical freshwater ecosystems. Environ. Microbiol. 11, 2339–2350 (2009).CAS 
    PubMed 

    Google Scholar 
    Newton, R. J., Jones, S. E., Eiler, A., McMahon, K. D. & Bertilsson, S. A guide to the natural history of freshwater lake Bacteria. Microbiol. Mol. Biol. Rev. 1, 1–10 (2011).
    Google Scholar 
    Parveen, B., Mary, I., Vellet, A., Ravet, V. & Debroas, D. Temporal dynamics and phylogenetic diversity of free-living and particle-associated Verrucomicrobia communities in relation to environmental variables in a mesotrophic lake. FEMS Microbiol. Ecol. 83, 189–201 (2013).CAS 
    PubMed 

    Google Scholar 
    Henson, M. W., Lanclos, V. C., Faircloth, B. C. & Thrash, J. C. Cultivation and genomics of the first freshwater SAR11 (LD12) isolate. ISME J. 12, 1846–1860 (2018).CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Yang, C. et al. The characteristics and algicidal mechanisms of cyanobactericidal bacteria, a review. World J. Microbiol. Biotechnol. 36, 1–10. https://doi.org/10.1007/s11274-020-02965-5 (2020).Article 

    Google Scholar 
    Izydorczyk, K. et al. Influence of abiotic and biotic factors on microcystin content in Microcystis aeruginosa cells in a eutrophic temperate reservoir. J. Plankton Res. 30, 393–400 (2008).CAS 

    Google Scholar 
    Mankiewicz-Boczek, J. et al. Bacteria homologus to Aeromonas capable of microcystin degradation. Open Life Sci. 10, 106–116 (2015).CAS 

    Google Scholar 
    Jaskulska, A., Font Nájera, A., Czarny, P., Serwecińska, L. & Mankiewicz-boczek, J. Daily dynamic of transcripts abundance of Ma-LMM01-like cyanophages in two lowland European reservoirs. Ecohydrol. Hydrobiol. 21, 543–548 (2021).
    Google Scholar 
    Gągała, I. et al. Role of environmental factors and toxic genotypes in the regulation of microcystins-producing cyanobacterial blooms. Microb. Ecol. 67, 465–479 (2014).PubMed 

    Google Scholar 
    Klindworth, A. et al. Evaluation of general 16S ribosomal RNA gene PCR primers for classical and next-generation sequencing-based diversity studies. Nucleic Acids Res. 41, 1–11 (2013).
    Google Scholar 
    Illumina. 16S Metagenomic Sequencing Library Preparation. (2013). http://support.illumina.com/content/dam/illumina-support/documents/documentation/chemistry_documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf.Frangeul, L. et al. Highly plastic genome of Microcystis aeruginosa PCC 7806, a ubiquitous toxic freshwater cyanobacterium. BMC Genomics 9, 1–20 (2008).
    Google Scholar 
    Hammer, Ø., Harper, D. A. T. & Ryan, P. D. Past: Paleontological statistics software package for education and data analysis even a cursory glance at the recent paleontological literature should convince anyone tha. Palaeontol. Electron. 4, 1–9 (2001).
    Google Scholar 
    Suzuki, M. T., Taylor, L. T. & DeLong, E. F. Quantitative analysis of small-subunit rRNA genes in mixed microbial populations via 5’-nuclease assays. Appl. Environ. Microbiol. 66, 4605–4614. https://doi.org/10.1128/AEM.66.11.4605-4614.2000 (2000).ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Neilan B. A et al. rRNA sequences and evolutionary relationships among toxic and nontoxic cyanobacteria of the genus Microcystis Int J Syst Bacteriol 47(3), 693–697, https://doi.org/10.1099/00207713-47-3-693 (1997).
    Google Scholar  More

  • in

    Building a truly diverse biodiversity science

    npj Biodiversity aims to be a common forum where discoveries in all areas of biodiversity science can be discussed, so that the research in specific topics with broad implications for other disciplines permeates the whole community. This requires that scientific debates are made in egalitarian terms between people with different backgrounds and points of view. We will strive to provide safe spaces where all biodiversity research can be showcased without bias, and theoretical and practical advances can be subject to calm and civil debate. As journal editors we will implement measures to work towards a fairer and more inclusive science, such as giving proper recognition to all researchers involved in the research published13, or ensuring in revisions that former research made by different identity groups and local scientists is adequately acknowledged14. We will also acknowledge diversity by maintaining a diverse editorial board15 and engaging external peer-reviewers16 that represent local specialists, the diversity of approaches in each field, as well as early-career researchers across demographic groups. We will also encourage access to research and engage in the FAIR principles for data management and sharing17. Here, good practice includes making data available for reanalysis or compilation in larger databases by researchers anywhere in the world, promoting open software, and sharing reproducible code18,19. Our hope is that this extends the capacity of developing meta-analyses and macroecological and macroevolutionary research beyond the borders of high-income countries.npj Biodiversity seeks to promote scientific discussion and synthesis. As editors, we will act as guides and moderators rather than as gatekeepers that merely decide which papers are above the threshold of publication20. Thus, we encourage debate as a central part of the editorial process, allowing well-grounded and clearly-identified speculation and policy-related statements in published papers when appropriate. This may include publishing non-conventional papers that foster discussion in established topics or open new research avenues21, if and only if they are well supported by data or published evidence. In this sense, we welcome Comments on areas currently under discussion, as well as Reviews and Perspectives that allow synthesis in theoretical and practical topics that are not necessarily general, but can help advance specific subdisciplines or topics. Last but not least, we want to facilitate communication between basic research and applied practitioners through Perspectives that translate the implications of recent research for management, conservation and adaptation to global change, or that identify which theoretical advances or additional empirical evidence would be needed to tackle specific problems.Creating the appropriate publishing environment for journals to be true forums for debate and provide value to the scientific community is a challenging enterprise. Above all, it requires escaping from the haste imposed by the “publish or perish model”, and making an explicit effort to raise the quality of the editorial process. In npj Biodiversity we will seek to follow ‘slow publishing’ principles, putting emphasis on meaningful debate between authors, editors and reviewers22. Current research environments can prevent researchers from having time to think, but true advance stems from digesting ideas and discussing them with the detail, depth and time they may need (http://slow-science.org/)23,24,25. Therefore, to contribute to a healthier, gentler and more thoughtful approach to biodiversity science, we will provide thorough and thoughtful reviews. We will make editorial decisions that, when paired with equally thorough and thoughtful work by authors, can reduce the number of times a paper bounces back and forth in successive rounds of peer review and revision. Note that this does not necessarily mean longer editorial times! Paradoxically, when authors, reviewers and editors commit to these “slow” publishing principles, the publication process can speed up. And most importantly, it will promote the spirit of productive debate that we aim for in npj Biodiversity. More

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    The fate of terrestrial biodiversity during an oceanic island volcanic eruption

    To our knowledge, this is the only work done on the terrestrial biodiversity status in the direct vicinity of a limited duration volcanic eruption. In this contribution, we document and assess the impact on the main plant and animal groups within the ecosystems during a volcanic eruption (Table 1). While some groups were clearly disadvantaged: ferns and herbaceous plants as well as invertebrates and saurians (lizards and geckos); other groups such as conifers and woody shrubs showed better resilience, as did the birds.This study is particularly important because of its location in a Mediterranean biodiversity hotspot13,14, harbouring a unique ecosystem of oceanic island organisms (38% of the Canary archipelago endemicity). Islands indeed exhibit a disproportionate amount of the world’s biodiversity but unfortunately a high number of extinctions have also occurred there14. The biodiversity in the south of the island is poorer than in the north. This is probably explained in part by the relatively frequent volcanic activity featuring seven major eruptions since 1585, including this one in 2021 (see15), which led to alternating destruction and neo-colonization processes.Concerning the flora, the Canary pine forest was the most affected ecosystem and vegetation type, as it is dominant in the vicinity of the new volcanic vents. The southern slopes of this forest were the most disturbed area due to the location of the volcano, combined with the prevailing northeasterly trade winds (Fig. 1). Tephra fallout and sulphurous gases were the main factors that affected the pine forest, over a vast surface area. Furthermore, the local xerophytic and thermophilous habitats also lost much of their surface area. In contrast to the pine forest, this drastic reduction was caused by the progressive downslope expansion of the lava flows.The Canary Island pine was thus notably affected by tephra fall, sulphuric acid aerosol12, and short episodes of acid rain. However, this conifer shows high resistance to temperature, confirming its great adaptation to volcanic events16, which is probably also one of the keys to its resistance to the more frequent present-day wildfires17. This pine species has evolved among volcanoes for the last 13 My16 and has adapted successfully to high temperatures. Moreover, thunderstorms with lightning occur in the Canaries together with abundant rainfall; consequently, wild forest fires should presumably not have been so frequent in the island’s past, before human colonization. In this habitat it is also remarkable that epiphytic lichens (U. articulata) apparently resisted on the pines until the 12th week, considering their high sensitivity to anthropogenic pollution18.The life cycle of flowering plants was drastically disrupted due to all the above factors, with great impact on foliage, photosynthesis, and growth. However, soil changes due to the deposition of tephra and its lixiviation by rain is one of the most dramatic factors affecting plants and a long-term impact of volcanic eruptions19. The nearest individuals to the crater were most directly affected by intense tephra falls and concentrated volcanic gases (SO2, HCl, HF, CO2). However, plants located in the nearest 200 m to the lava flows but at more than 2 km from the crater were presumably more disturbed by the high temperature of the slow-cooling lava and its lesser gas emissions.Large woody plants exhibited a better frequency of survival than smaller ones in the face of this extreme stress (Table S1 and19). In the Hekla area (Iceland), most trees have thickened trunks, indicating that those trees that survive have had a long life subjected to frequent volcanic damage19. Secondary woodiness of island plants (sensu20) has been traditionally related to drought20,21, ecological shift22 or a counter-selection of inbreeding depression in founding island populations23. However, this adaptation also favours the resistance of many shrubby plants to high temperatures close to craters and lava flows but primarily their resistance to the intense tephra falls that affect a much larger area. In addition, plant and stem height plays a fundamental role in overcoming the deep layers of deposits. This latter effect was particularly important up to 2.5 km from the crater (tephra thickness  > 30 cm) (Figs. 1 and 2), as the herbaceous plants were completely buried, sometimes to more than 1.5 m depth. Therefore, the seed bank has also probably been rendered largely non-functional. However, deposits were recorded over almost the whole island, indicating that longer lasting or more intense eruptions would severely affect an even larger area. Such events have been hitherto ignored in the intensely discussed “island woodiness” debate21,23,24,25,26,27. We found surviving populations of endemic woody taxa heavily impacted by tephra deposits close to lava flows, across a wide range of genera such as Rumex (R. lunaria), Echium (E. brevirame), Euphorbia (E. lamarckii, E. canariensis and E. balsamifera), Aeonium (A. davidbramwellii), Rubia (R. fruticosa), Schizogyne (S. sericea), Carlina (C. falcata) or Sonchus (S. hierrensis) (Table S2), which coincide with the general list of woody Canary plants20. Most members of these genera in other ecosystems on continents are mainly herbaceous. As such eruptions and their impacts due to ash depositions are frequent events on volcanic islands, e.g. several times within a century on La Palma, this is a “frequent” selective process at evolutionary time scales.With regard to the fauna, the invertebrate community collapsed during the first two weeks (Table S2), probably due to rapid deterioration of the growth state of plants. These changes in the invertebrates were caused by the tephra contacting the cuticular lipid layer28 and water loss due to tegument abrasion29. In this period, many insect pests (especially whitefly pupae) in banana plantations (farmers’ observations) were drastically reduced. This sudden decrease in insect populations affected the whole food web and probably caused part of the ecological collapse of saurian and some passerine communities30. In the case of lizards, smaller individuals seem to resist the adverse conditions better than large ones, as observed in other eruptions3. This could be linked to their lower food requirements and greater ease in finding refuges. Loss of body condition in lizards post-eruption has been recorded and negatively affects reproduction quality31. However, some lizards have shown a good ability to find food in the tephra substrate32. We found abundant tephra particles in some vertebrate droppings (lizards, birds, and mammals) during the eruption, probably involuntarily ingested. At least in bats, ingestion during feeding produces physiological stress that is likely related to baldness, high ectoparasite loads or possible mineral deficiencies33.As described in the Canary Islands, some passerines show high fidelity to their territories (see34). During the eruption, Sardinian warblers (Curruca melanocephala) maintained their territories until the imminent arrival of lava flows. Larger birds (kestrels F. tinnunculus, ravens C. corax and buzzards B. buteo) were well able to continue flying in the areas surrounding the crater. Furthermore, some cases like F. tinnunculus showed great feeding plasticity in the first couple of weeks. At least six times, kestrels tried to catch birds (especially small passerines and doves), contrary to their usual diet based on abundant lizards and insects35. Widening of trophic niches in island organisms has traditionally been interpreted as linked to disharmony in island ecosystems36,37,38. However, this plasticity is tremendously beneficial in ecological catastrophes, where food becomes exceptionally scarce. In the case of bats, their flight is limited by the delicate structure of their patagium, which can be damaged by the frequent pyroclastic tephra fall. Furthermore, scarcity of insects in the first few kilometres from the crater probably led to their displacement to other more distant and richer food resource zones.As we learned from the movement capacity of the vertebrate animals that still inhabited the affected area, those with greater mobility, birds and bats, resisted the eruptive process much better than those with less mobility, e.g. saurians.Lastly, during this destructive event on La Palma, we had the opportunity to increase our knowledge of how ecological-evolutionary adaptations have favoured the survival of insular organisms. Such responses are traditionally mentioned in the context of island biology. As already mentioned, one of the most interesting findings verifies the remarkable adaptation of Canary Island pine trees (P. canariensis) to volcanism (see16), including extremely harsh ecological conditions. Other insular trends related to the prevalence of woodiness in insular flowering plants20,21, or the high trophic plasticity of some vertebrates on oceanic islands36, have not previously been associated with their potential evolution along with volcanic processes. However, such evolutionary adaptations most likely played an important role in the survival of plants and animals affected by the volcano. For this reason, it is worth considering and debating whether these previously mentioned evolutionary processes are in fact also linked to repeated volcanic episodes on oceanic islands. More

  • in

    Nitrogen-fixing symbiotic bacteria act as a global filter for plant establishment on islands

    Delavaux, C. S., Smith‐Ramesh, L. M. & Kuebbing, S. E. Beyond nutrients: a meta‐analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98, 2111–2119 (2017).Lugtenberg, B. & Kamilova, F. Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63, 541–556 (2009).Article 
    CAS 
    PubMed 

    Google Scholar 
    Franche, C., Lindström, K. & Elmerich, C. Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321, 35–59 (2009).Article 
    CAS 

    Google Scholar 
    Razanajatovo, M. et al. Autofertility and self‐compatibility moderately benefit island colonization of plants. Glob. Ecol. Biogeogr. 28, 341–352 (2019).Article 

    Google Scholar 
    Schrader, J., Wright, I. J., Kreft, H. & Westoby, M. A roadmap to plant functional island biogeography. Biol. Rev. (2021).Herridge, D. F., Peoples, M. B. & Boddey, R. M. Global inputs of biological nitrogen fixation in agricultural systems. Plant Soil 311, 1–18 (2008).Article 
    CAS 

    Google Scholar 
    Vitousek, P. Nutrient cycling and limitation: Hawai’i as a model ecosystem. (Princeton Univ. Press, Princeton, NJ, 2004). Nutrient cycling and limitation: Hawai’i as a model ecosystem. Princeton Univ. Press, Princeton, NJ.Book 

    Google Scholar 
    Becking, L. G. M. B. Geobiologie of inleiding tot de milieukunde. (WP Van Stockum & Zoon, 1934).Peay, K. G. & Bruns, T. D. Spore dispersal of basidiomycete fungi at the landscape scale is driven by stochastic and deterministic processes and generates variability in plant–fungal interactions. N. Phytol. 204, 180–191 (2014).Article 

    Google Scholar 
    Delavaux, C. S. et al. Mycorrhizal fungi influence global plant biogeography. Nat. Ecol. Evol. 3, 424 (2019).Article 
    PubMed 

    Google Scholar 
    Duchicela, J., Bever, J. D. & Schultz, P. A. Symbionts as Filters of Plant Colonization of Islands: Tests of Expected Patterns and Environmental Consequences in the Galapagos. Plants 9, 74 (2020).Article 
    CAS 
    PubMed Central 

    Google Scholar 
    Delavaux, C. S. et al. Mycorrhizal types influence island biogeography of plants. Commun. Biol. 4, 1–8 (2021).Article 

    Google Scholar 
    Simonsen, A. K., Dinnage, R., Barrett, L. G., Prober, S. M. & Thrall, P. H. Symbiosis limits establishment of legumes outside their native range at a global scale. Nat. Commun. 8, 1–9 (2017).Article 

    Google Scholar 
    Poole, P., Ramachandran, V. & Terpolilli, J. Rhizobia: from saprophytes to endosymbionts. Nat. Rev. Microbiol. 16, 291–303 (2018).Article 
    CAS 
    PubMed 

    Google Scholar 
    Sprent, J. I., Ardley, J. & James, E. K. Biogeography of nodulated legumes and their nitrogen‐fixing symbionts. N. Phytol. 215, 40–56 (2017).Article 
    CAS 

    Google Scholar 
    Menge, D. N. Hedin, L. O. & Pacala, S. W. Nitrogen and phosphorus limitation over long-term ecosystem development in terrestrial ecosystems. (2012).Lambers, H., Raven, J. A., Shaver, G. R. & Smith, S. E. Plant nutrient-acquisition strategies change with soil age. Trends Ecol. evolution 23, 95–103 (2008).Article 

    Google Scholar 
    Walker, T. & Syers, J. K. The fate of phosphorus during pedogenesis. Geoderma 15, 1–19 (1976).Article 
    CAS 

    Google Scholar 
    Jin, L. et al. Synergistic interactions of arbuscular mycorrhizal fungi and rhizobia promoted the growth of Lathyrus sativus under sulphate salt stress. Symbiosis 50, 157–164 (2010).Article 
    CAS 

    Google Scholar 
    Afkhami, M. E. & Stinchcombe, J. R. Multiple mutualist effects on genomewide expression in the tripartite association between Medicago truncatula, nitrogen‐fixing bacteria and mycorrhizal fungi. Mol. Ecol. 25, 4946–4962 (2016).Article 
    CAS 
    PubMed 

    Google Scholar 
    Larimer, A. L., Clay, K. & Bever, J. D. Synergism and context dependency of interactions between arbuscular mycorrhizal fungi and rhizobia with a prairie legume. Ecology 95, 1045–1054 (2014).Article 
    PubMed 

    Google Scholar 
    Primieri, S., Magnoli, S. M., Koffel, T. S., Stürmer, S. L. & Bever, J. D. Perennial, but not annual legumes synergistically benefit from infection with arbuscular mycorrhizal fungi and rhizobia: a meta‐analysis. N. Phytol. 233, 505-514 (2021).Larimer, A. L., Bever, J. D. & Clay, K. The interactive effects of plant microbial symbionts: a review and meta-analysis. Symbiosis 51, 139–148 (2010).Article 

    Google Scholar 
    Werner, G. D., Cornwell, W. K., Sprent, J. I., Kattge, J. & Kiers, E. T. A single evolutionary innovation drives the deep evolution of symbiotic N 2-fixation in angiosperms. Nat. Commun. 5, 1–9 (2014).Article 

    Google Scholar 
    Weigelt, P., König, C. & Kreft, H. GIFT- A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020).Article 

    Google Scholar 
    Werner, G. D. et al. Symbiont switching and alternative resource acquisition strategies drive mutualism breakdown. Proc. Natl Acad. Sci. 115, 5229–5234 (2018).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bamba, M. et al. Wide distribution range of rhizobial symbionts associated with pantropical sea-dispersed legumes. Antonie van. Leeuwenhoek 109, 1605–1614 (2016).Article 
    PubMed 

    Google Scholar 
    Chen, W.-M., Lee, T.-M., Lan, C.-C. & Cheng, C.-P. Characterization of halotolerant rhizobia isolated from root nodules of Canavalia rosea from seaside areas. FEMS Microbiol. Ecol. 34, 9–16 (2000).Article 
    CAS 
    PubMed 

    Google Scholar 
    Toma, M. A. et al. Tripartite symbiosis of Sophora tomentosa, rhizobia and arbuscular mycorhizal fungi. Braz. J. Microbiol. 48, 680–688 (2017).Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Elanchezhian, R., Rajalakshmi, S. & Jayakumar, V. Salt tolerance characteristics of rhizobium species associated with Vigna marina. Indian J. Agric. Sci. 79, 980–985 (2009).CAS 

    Google Scholar 
    Chapin, F. S., Matson, P. A., Mooney, H. A. & Vitousek, P. M. Principles of Terrestrial Ecosystem Ecology (Springer, 2002).Vitousek, P. M., Walker, L. R., Whiteaker, L. D. & Matson, P. A. Nutrient limitations to plant growth during primary succession in Hawaii Volcanoes National Park. Biogeochemistry 23, 197–215 (1993).Article 

    Google Scholar 
    Liao, C. et al. Altered ecosystem carbon and nitrogen cycles by plant invasion: a meta-analysis. N. Phytologist 177, 706–714 (2008).Article 
    CAS 

    Google Scholar 
    Woodward, S. A. et al. Use of the Exotic Tree Myrica Faya by Native and Exotic Birds in Hawai’i Volcanoes National Park (University of Hawaii Press, 1990).Vitousek, P. M., Walker, L. R., Whiteaker, L. D., Mueller-Dombois, D. & Matson, P. A. Biological invasion by Myrica faya alters ecosystem development in Hawaii. Science 238, 802–804 (1987).Article 
    CAS 
    PubMed 

    Google Scholar 
    Theoharides, K. A. & Dukes, J. S. Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. N. phytologist 176, 256–273 (2007).Article 

    Google Scholar 
    Kalwij, J. M. Review of ‘The Plant List, a working list of all plant species’. J. Vegetation Sci. 23, 998–1002 (2012).Article 

    Google Scholar 
    Byng, J. W. et al. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical J. Linn. Soc. 181, 1–20 (2016).Article 

    Google Scholar 
    Soudzilovskaia, N. A. et al. FungalRoot: Global online database of plant mycorrhizal associations. N. Phytol. 227, 955–966 (2020).Article 

    Google Scholar 
    Weigelt, P., König, C. & Kreft, H. GIFT–A global inventory of floras and traits for macroecology and biogeography. J. Biogeogr. 47, 16–43 (2020).Article 

    Google Scholar 
    Karger, D. N. et al. Climatologies at high resolution for the earth’s land surface areas. Sci. Data 4, 170122 (2017).Article 
    PubMed 
    PubMed Central 

    Google Scholar 
    Danielson, J. J. & Gesch, D. B. “Global multi-resolution terrain elevation data 2010 (GMTED2010),” (US Geological Survey, 2011).Weigelt, P. & Kreft, H. Quantifying island isolation–insights from global patterns of insular plant species richness. Ecography 36, 417–429 (2013).Article 

    Google Scholar 
    Kreft, H., Jetz, W., Mutke, J., Kier, G. & Barthlott, W. Global diversity of island floras from a macroecological perspective. Ecol. Lett. 11, 116–127 (2008).PubMed 

    Google Scholar 
    Triantis, K. A., Economo, E. P., Guilhaumon, F. & Ricklefs, R. E. Diversity regulation at macro‐scales: species richness on oceanic archipelagos. Glob. Ecol. Biogeogr. 24, 594–605 (2015).Article 

    Google Scholar 
    Crase, B., Liedloff, A. C. & Wintle, B. A. A new method for dealing with residual spatial autocorrelation in species distribution models. Ecography 35, 879–888 (2012).Article 

    Google Scholar 
    Bivand, R. R packages for analyzing spatial data: a comparative case study with areal data. Geogr. Anal. 54, 488–518 (2022).Article 

    Google Scholar 
    R. C. Team, R: A language and environment for statistical computing. (R Foundation for Statistical Computing, 2019).Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 67, 1–48 (2015).Article 

    Google Scholar  More

  • in

    Abundant and cosmopolitan lineage of cyanopodoviruses lacking a DNA polymerase gene

    Suttle CA. Marine viruses-major players in the global ecosystem. Nat Rev Microbiol. 2007;5:801–12.CAS 
    PubMed 

    Google Scholar 
    Fuhrman JA. Marine viruses and their biogeochemical and ecological effects. Nature 1999;399:541–8.CAS 
    PubMed 

    Google Scholar 
    Rohwer F, Thurber RV. Viruses manipulate the marine environment. Nature 2009;459:207–12.CAS 
    PubMed 

    Google Scholar 
    Breitbart M, Bonnain C, Malki K, Sawaya NA. Phage puppet masters of the marine microbial realm. Nat Microbiol. 2018;3:754–66.CAS 
    PubMed 

    Google Scholar 
    Zimmerman AE, Howard-Varona C, Needham DM, John SG, Worden AZ, Sullivan MB, et al. Metabolic and biogeochemical consequences of viral infection in aquatic ecosystems. Nat Rev Microbiol. 2020;18:21–34.CAS 
    PubMed 

    Google Scholar 
    Rosenwasser S, Ziv C, Creveld SGV, Vardi A. Virocell metabolism: metabolic innovations during host-virus interactions in the ocean. Trends Microbiol. 2016;24:821–32.CAS 
    PubMed 

    Google Scholar 
    Fuchsman CA, Carlson MCG, Garcia Prieto D, Hays MD, Rocap G. Cyanophage host-derived genes reflect contrasting selective pressures with depth in the oxic and anoxic water column of the Eastern Tropical North Pacific. Environ Microbiol. 2021;23:2782–2800.CAS 
    PubMed 

    Google Scholar 
    Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, et al. Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 2016;537:689–93.CAS 
    PubMed 

    Google Scholar 
    Gregory AC, Zayed AA, Conceição-Neto N, Temperton B, Bolduc B, Alberti A, et al. Marine DNA viral macro-and microdiversity from pole to pole. Cell 2019;177:1109–23.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, et al. Patterns and ecological drivers of ocean viral communities. Science 2015;348:1261498.PubMed 

    Google Scholar 
    Dion MB, Oechslin F, Moineau S. Phage diversity, genomics and phylogeny. Nat Rev Microbiol. 2020;18:125–38.CAS 
    PubMed 

    Google Scholar 
    Sullivan MB, Waterbury JB, Chisholm SW. Cyanophages infecting the oceanic cyanobacterium Prochlorococcus. Nature 2003;424:1047–51.CAS 
    PubMed 

    Google Scholar 
    Mann NH. Phages of the marine cyanobacterial picophytoplankton. FEMS Microbiol Rev. 2003;27:17–34.CAS 
    PubMed 

    Google Scholar 
    Ni T, Zeng Q. Diel infection of cyanobacteria by cyanophages. Front Mar Sci. 2016;2:123.
    Google Scholar 
    Flombaum P, Gallegos JL, Gordillo RA, Rincon J, Zabala LL, Jiao N, et al. Present and future global distributions of the marine Cyanobacteria Prochlorococcus and Synechococcus. Proc Natl Acad Sci USA 2013;110:9824–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Biller SJ, Berube PM, Lindell D, Chisholm SW. Prochlorococcus: the structure and function of collective diversity. Nat Rev Microbiol 2015;13:13–27.CAS 
    PubMed 

    Google Scholar 
    Proctor LM, Fuhrman JA. Viral mortality of marine-bacteria and cyanobacteria. Nature 1990;343:60–62.
    Google Scholar 
    Carlson MCG, Ribalet F, Maidanik I, Durham BP, Hulata Y, Ferron S, et al. Viruses affect picocyanobacterial abundance and biogeography in the North Pacific Ocean. Nat Microbiol 2022;7:570–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Matteson AR, Loar SN, Pickmere S, DeBruyn JM, Ellwood MJ, Boyd PW, et al. Production of viruses during a spring phytoplankton bloom in the South Pacific Ocean near of New Zealand. FEMS Microbiol Ecol 2012;79:709–19.CAS 
    PubMed 

    Google Scholar 
    Ribalet F, Swalwell J, Clayton S, Jimenez V, Sudek S, Lin Y, et al. Light-driven synchrony of Prochlorococcus growth and mortality in the subtropical Pacific gyre. Proc Natl Acad Sci USA. 2015;112:8008–12.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Demory D, Liu R, Chen Y, Zhao F, Coenen AR, Zeng Q, et al. Linking light-dependent life history traits with population dynamics for Prochlorococcus and cyanophage. mSystems 2020;5:e00586–19.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D. Genomic island variability facilitates Prochlorococcus-virus coexistence. Nature 2011;474:604–8.CAS 
    PubMed 

    Google Scholar 
    Marston MF, Pierciey FJ Jr, Shepard A, Gearin G, Qi J, Yandava C, et al. Rapid diversification of coevolving marine Synechococcus and a virus. Proc Natl Acad Sci USA 2012;109:4544–9.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xiao X, Guo W, Li X, Wang C, Chen X, Lin X, et al. Viral lysis alters the optical properties and biological availability of dissolved organic matter derived from Prochlorococcus picocyanobacteria. Appl Environ Microbiol. 2021;87:e02271–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Xiao X, Zeng Q, Zhang R, Jiao N. Prochlorococcus viruses—From biodiversity to biogeochemical cycles. Sci China Earth Sci. 2018;61:1728–36.
    Google Scholar 
    Jover LF, Effler TC, Buchan A, Wilhelm SW, Weitz JS. The elemental composition of virus particles: implications for marine biogeochemical cycles. Nat Rev Microbiol. 2014;12:519–28.CAS 
    PubMed 

    Google Scholar 
    Puxty RJ, Millard AD, Evans DJ, Scanlan DJ. Viruses inhibit CO2 fixation in the most abundant phototrophs on earth. Curr Biol 2016;26:1585–9.CAS 
    PubMed 

    Google Scholar 
    Weitz JS, Stock CA, Wilhelm SW, Bourouiba L, Coleman ML, Buchan A, et al. A multitrophic model to quantify the effects of marine viruses on microbial food webs and ecosystem processes. ISME J. 2015;9:1352–64.PubMed 
    PubMed Central 

    Google Scholar 
    Sullivan MB, Coleman ML, Weigele P, Rohwer F, Chisholm SW. Three Prochlorococcus cyanophage genomes: signature features and ecological interpretations. PLoS Biol. 2005;3:e144.PubMed 
    PubMed Central 

    Google Scholar 
    Sullivan MB, Krastins B, Hughes JL, Kelly L, Chase M, Sarracino D, et al. The genome and structural proteome of an ocean siphovirus: a new window into the cyanobacterial ‘mobilome’. Environ Microbiol. 2009;11:2935–51.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sullivan MB, Huang KH, Ignacio-Espinoza JC, Berlin AM, Kelly L, Weigele PR, et al. Genomic analysis of oceanic cyanobacterial myoviruses compared with T4-like myoviruses from diverse hosts and environments. Environ Microbiol. 2010;12:3035–56.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Sabehi G, Shaulov L, Silver DH, Yanai I, Harel A, Lindell D. A novel lineage of myoviruses infecting cyanobacteria is widespread in the oceans. Proc Natl Acad Sci USA 2012;109:2037–42.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huang S, Wang K, Jiao N, Chen F. Genome sequences of siphoviruses infecting marine Synechococcus unveil a diverse cyanophage group and extensive phage-host genetic exchanges. Environ Microbiol. 2012;14:540–58.CAS 
    PubMed 

    Google Scholar 
    Labrie SJ, Frois-Moniz K, Osburne MS, Kelly L, Roggensack SE, Sullivan MB, et al. Genomes of marine cyanopodoviruses reveal multiple origins of diversity. Environ Microbiol. 2013;15:1356–76.CAS 
    PubMed 

    Google Scholar 
    Dekel-Bird NP, Avrani S, Sabehi G, Pekarsky I, Marston MF, Kirzner S, et al. Diversity and evolutionary relationships of T7-like podoviruses infecting marine cyanobacteria. Environ Microbiol. 2013;15:1476–91.CAS 
    PubMed 

    Google Scholar 
    Huang S, Wilhelm SW, Jiao N, Chen F. Ubiquitous cyanobacterial podoviruses in the global oceans unveiled through viral DNA polymerase gene sequences. ISME J. 2010;4:1243–51.PubMed 

    Google Scholar 
    Baran N, Goldin S, Maidanik I, Lindell D. Quantification of diverse virus populations in the environment using the polony method. Nat Microbiol. 2018;3:62–72.CAS 
    PubMed 

    Google Scholar 
    Chow C-ET, Suttle CA. Biogeography of viruses in the sea. Annu Rev Virol. 2015;2:41–66.CAS 
    PubMed 

    Google Scholar 
    Chen F, Lu JR. Genomic sequence and evolution of marine cyanophage P60: a new insight on lytic and lysogenic phages. Appl Environ Microbiol. 2002;68:2589–94.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huang S, Zhang S, Jiao N, Chen F. Comparative genomic and phylogenomic analyses reveal a conserved core genome shared by estuarine and oceanic cyanopodoviruses. PLoS One. 2015;10:e0142962.PubMed 
    PubMed Central 

    Google Scholar 
    Pope WH, Weigele PR, Chang J, Pedulla ML, Ford ME, Houtz JM, et al. Genome sequence, structural proteins, and capsid organization of the cyanophage Syn5: A “horned’ bacteriophage of marine Synechococcus. J Mol Biol. 2007;368:966–81.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Huang S, Sun Y, Zhang S, Long L. Temporal transcriptomes of a marine cyanopodovirus and its Synechococcus host during infection. Microbiologyopen 2021;10:e1150.CAS 
    PubMed 

    Google Scholar 
    Wang K, Chen F. Prevalence of highly host-specific cyanophages in the estuarine environment. Environ Microbiol. 2008;10:300–12.CAS 
    PubMed 

    Google Scholar 
    Chen F, Wang K, Huang S, Cai H, Zhao M, Jiao N, et al. Diverse and dynamic populations of cyanobacterial podoviruses in the Chesapeake Bay unveiled through DNA polymerase gene sequences. Environ Microbiol. 2009;11:2884–92.PubMed 

    Google Scholar 
    Goldin S, Hulata Y, Baran N, Lindell D. Quantification of T4-like and T7-like cyanophages using the polony method show they are significant members of the virioplankton in the North Pacific Subtropical Gyre. Front Microbiol. 2020;11:1210.PubMed 
    PubMed Central 

    Google Scholar 
    Nasko DJ, Chopyk J, Sakowski EG, Ferrell BD, Polson SW, Wommack KE. Family A DNA polymerase phylogeny uncovers diversity and replication gene organization in the virioplankton. Front Microbiol. 2018;9:3053.PubMed 
    PubMed Central 

    Google Scholar 
    Dekel-Bird NP, Sabehi G, Mosevitzky B, Lindell D. Host-dependent differences in abundance, composition and host range of cyanophages from the Red Sea. Environ Microbiol. 2015;17:1286–99.CAS 
    PubMed 

    Google Scholar 
    Hanson CA, Marston MF, Martiny JBH. Biogeographic variation in host range phenotypes and taxonomic composition of marine cyanophage isolates. Front Microbiol. 2016;7:983.PubMed 
    PubMed Central 

    Google Scholar 
    Rocap G, Larimer FW, Lamerdin J, Malfatti S, Chain P, Ahlgren NA, et al. Genome divergence in two Prochlorococcus ecotypes reflects oceanic niche differentiation. Nature 2003;424:1042–7.CAS 
    PubMed 

    Google Scholar 
    Chen B, Wang L, Song S, Huang B, Sun J, Liu H. Comparisons of picophytoplankton abundance, size, and fluorescence between summer and winter in northern South China Sea. Cont Shelf Res. 2011;31:1527–40.
    Google Scholar 
    Lindell D, Jaffe JD, Coleman ML, Futschik ME, Axmann IM, Rector T, et al. Genome-wide expression dynamics of a marine virus and host reveal features of co-evolution. Nature 2007;449:83–86.CAS 
    PubMed 

    Google Scholar 
    Zhao Y, Qin F, Zhang R, Giovannoni SJ, Zhang Z, Sun J, et al. Pelagiphages in the Podoviridae family integrate into host genomes. Environ Microbiol. 2019;21:1989–2001.CAS 
    PubMed 

    Google Scholar 
    Leptihn S, Gottschalk J, Kuhn A. T7 ejectosome assembly: A story unfolds. Bacteriophage 2016;6:e1128513.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Thompson LR, Zeng Q, Kelly L, Huang KH, Singer AU, Stubbe J, et al. Phage auxiliary metabolic genes and the redirection of cyanobacterial host carbon metabolism. Proc Natl Acad Sci USA 2011;108:E757–64.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zeng Q, Chisholm SW. Marine viruses exploit their host’s two-component regulatory system in response to resource limitation. Curr Biol 2012;22:124–8.CAS 
    PubMed 

    Google Scholar 
    Zeng Q, Bonocora RP, Shub DA. A free-standing homing endonuclease targets an intron insertion site in the psbA gene of cyanophages. Curr Biol. 2009;19:218–22.CAS 
    PubMed 

    Google Scholar 
    Lindell D, Jaffe JD, Johnson ZI, Church GM, Chisholm SW. Photosynthesis genes in marine viruses yield proteins during host infection. Nature 2005;438:86–89.CAS 
    PubMed 

    Google Scholar 
    Breitbart M, Thompson LR, Suttle CA, Sullivan MB. Exploring the vast diversity of marine viruses. Oceanography. 2007;20:135–9.
    Google Scholar 
    Kazlauskas D, Venclovas C. Computational analysis of DNA replicases in double-stranded DNA viruses: relationship with the genome size. Nucleic Acids Res. 2011;39:8291–305.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu X, Zhang Q, Murata K, Baker ML, Sullivan MB, Fu C, et al. Structural changes in a marine podovirus associated with release of its genome into Prochlorococcus. Nat Struct Mol Biol. 2010;17:830–6.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Dai W, Fu C, Raytcheva D, Flanagan J, Khant HA, Liu XG, et al. Visualizing virus assembly intermediates inside marine cyanobacteria. Nature 2013;502:707–10.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Liu R, Liu Y, Chen Y, Zhan Y, Zeng Q. Cyanobacterial viruses exhibit diurnal rhythms during infection. Proc Natl Acad Sci USA 2019;116:14077–82.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Maidanik I, Kirzner S, Pekarski I, Arsenieff L, Tahan R, Carlson MCG, et al. Cyanophages from a less virulent clade dominate over their sister clade in global oceans. ISME J. 2022;16:2169–80.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Shitrit D, Hackl T, Laurenceau R, Raho N, Carlson MCG, Sabehi G, et al. Genetic engineering of marine cyanophages reveals integration but not lysogeny in T7-like cyanophages. ISME J. 2022;16:488–99.CAS 
    PubMed 

    Google Scholar 
    Liang Y, Wang L, Wang Z, Zhao J, Yang Q, Wang M, et al. Metagenomic analysis of the diversity of DNA viruses in the surface and deep sea of the South China Sea. Front Microbiol. 2019;10:1951.PubMed 
    PubMed Central 

    Google Scholar 
    Pedrós-Alió C, Potvin M, Lovejoy C. Diversity of planktonic microorganisms in the Arctic Ocean. Prog Oceanogr. 2015;139:233–43.
    Google Scholar 
    Luo E, Eppley JM, Romano AE, Mende DR, DeLong EF. Double-stranded DNA virioplankton dynamics and reproductive strategies in the oligotrophic open ocean water column. ISME J. 2020;14:1304–15.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Steidinger BS, Crowther TW, Liang J, Van Nuland ME, Werner GDA, Reich PB, et al. Climatic controls of decomposition drive the global biogeography of forest-tree symbioses. Nature 2019;569:404–8.CAS 
    PubMed 

    Google Scholar 
    Xie X, Wu T, Zhu M, Jiang G, Xu Y, Wang X, et al. Comparison of random forest and multiple linear regression models for estimation of soil extracellular enzyme activities in agricultural reclaimed coastal saline land. Ecol Indic. 2021;120:106925.CAS 

    Google Scholar 
    Lee SJ, Richardson CC. Choreography of bacteriophage T7 DNA replication. Curr Opin Chem Biol. 2011;15:580–6.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Kulczyk AW, Richardson CC. The replication system of bacteriophage T7. Enzymes. 2016;39:89–136.CAS 
    PubMed 

    Google Scholar 
    Benkovic SJ, Valentine AM, Salinas F. Replisome-mediated DNA replication. Annu Rev Biochem. 2001;70:181–208.CAS 
    PubMed 

    Google Scholar 
    Johnson A, O’Donnell M. Cellular DNA replicases: components and dynamics at the replication fork. Annu Rev Biochem. 2005;74:283–315.CAS 
    PubMed 

    Google Scholar 
    Seco EM, Zinder JC, Manhart CM, Lo Piano A, McHenry CS, Ayora S. Bacteriophage SPP1 DNA replication strategies promote viral and disable host replication in vitro. Nucleic Acids Res. 2013;41:1711–21.CAS 
    PubMed 

    Google Scholar 
    Mruwat N, Carlson MCG, Goldin S, Ribalet F, Kirzner S, Hulata Y, et al. A single-cell polony method reveals low levels of infected Prochlorococcus in oligotrophic waters despite high cyanophage abundances. ISME J. 2021;15:41–54.CAS 
    PubMed 

    Google Scholar 
    Moore LR, Rocap G, Chisholm SW. Physiology and molecular phylogeny of coexisting Prochlorococcus ecotypes. Nature 1998;393:464–7.CAS 
    PubMed 

    Google Scholar 
    Puxty RJ, Millard AD, Evans DJ, Scanlan DJ. Shedding new light on viral photosynthesis. Photosynth Res. 2015;126:71–97.CAS 
    PubMed 

    Google Scholar 
    Edwards KF, Steward GF, Schvarcz CR. Making sense of virus size and the tradeoffs shaping viral fitness. Ecol Lett. 2021;24:363–73.PubMed 

    Google Scholar 
    Moore LR, Coe A, Zinser ER, Saito MA, Sullivan MB, Lindell D, et al. Culturing the marine cyanobacterium Prochlorococcus. Limnol Oceanogr Methods. 2007;5:353–62.CAS 

    Google Scholar 
    Hyman P, Abedon ST. Bacteriophage host range and bacterial resistance. Adv Appl Microbiol. 2010;70:217–48.CAS 
    PubMed 

    Google Scholar 
    Fridman S, Flores-Uribe J, Larom S, Alalouf O, Liran O, Yacoby I, et al. A myovirus encoding both photosystem I and II proteins enhances cyclic electron flow in infected Prochlorococcus cells. Nat Microbiol. 2017;2:1350–7.CAS 
    PubMed 

    Google Scholar 
    Fang X, Liu Y, Zhao Y, Chen Y, Liu R, Qin QL, et al. Transcriptomic responses of the marine cyanobacterium Prochlorococcus to viral lysis products. Environ Microbiol. 2019;21:2015–28.CAS 
    PubMed 

    Google Scholar 
    John SG, Mendez CB, Deng L, Poulos B, Kauffman AK, Kern S, et al. A simple and efficient method for concentration of ocean viruses by chemical flocculation. Environ Microbiol Rep. 2011;3:195–202.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014;30:2114–20.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics 2011;27:863–4.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:1–10.
    Google Scholar 
    Peng Y, Leung HC, Yiu SM, Chin FY. IDBA-UD: a de novo assembler for single-cell and metagenomic sequencing data with highly uneven depth. Bioinformatics 2012;28:1420–8.CAS 
    PubMed 

    Google Scholar 
    Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 2014;30:2068–9.CAS 
    PubMed 

    Google Scholar 
    Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–7.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic Inference in the genomic era. Mol Biol Evol. 2020;37:2461–2461.PubMed 
    PubMed Central 

    Google Scholar 
    Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22.CAS 
    PubMed 

    Google Scholar 
    Martinez-Hernandez F, Fornas O, Lluesma Gomez M, Bolduc B, de la Cruz Pena MJ, Martinez JM, et al. Single-virus genomics reveals hidden cosmopolitan and abundant viruses. Nat Commun. 2017;8:15892.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Zhang Z, Qin F, Chen F, Chu X, Luo H, Zhang R, et al. Culturing novel and abundant pelagiphages in the ocean. Environ Microbiol 2021;23:1145–61.CAS 
    PubMed 

    Google Scholar 
    Buchholz HH, Michelsen ML, Bolanos LM, Browne E, Allen MJ, Temperton B. Efficient dilution-to-extinction isolation of novel virus-host model systems for fastidious heterotrophic bacteria. ISME J. 2021;15:1585–98.CAS 
    PubMed 
    PubMed Central 

    Google Scholar 
    Qin F, Du S, Zhang Z, Ying H, Wu Y, Zhao G, et al. Newly identified HMO-2011-type phages reveal genomic diversity and biogeographic distributions of this marine viral group. ISME J. 2022;16:1363–75.CAS 
    PubMed 
    PubMed Central 

    Google Scholar  More