Using Margalef’s vision to understand the current aquatic microbial ecology

  1. Borrero-Santiago, Ana Rocio
  2. Dellisanti, Walter
  3. Sánchez-Quinto, Andrés
  4. Moreno-Andrés, Javier
  5. Nemoy, Philip
  6. Richa, Kumari
  7. Valdespino-Castillo, Patricia Margarita
  8. Diaz-de-Quijano, Daniel
  9. Ontiveros, Vicente J.
  10. Fontana, Simone
  11. Giner, Caterina R.
  12. Sanz-Sáez, Isabel
  13. Mestre, Mireia
Revista:
Scientia Marina

ISSN: 0214-8358

Año de publicación: 2022

Volumen: 86

Número: 1

Tipo: Artículo

DOI: 10.3989/SCIMAR.05199.026 DIALNET GOOGLE SCHOLAR lock_openAcceso abierto editor

Otras publicaciones en: Scientia Marina

Resumen

Ramon Margalef fue un científico pionero que introdujo un enfoque interdisciplinario a los estudios ecológicos. Sus estudios fueron de los primeros en incorporar diferentes conceptos en la literatura de la ecología acuática, desde los organismos y las interacciones de los ecosistemas hasta la evolución. Para llevar el enfoque de Margalef a los estudios científicos actuales, en este articulo exploramos su visión de la ecología acuática dentro de cuatro campos de estudio interrelacionados: teoría ecológica, diversidad microbiana, ciclos biogeoquímicos y cambios ambientales globales. Inspirándonos en sus estudios pasados, analizamos en este texto los desafíos científicos actuales y proponemos un enfoque integrado considerando el concepto unificador del Mandala de Margalef con el objetivo de mejorar los estudios futuros sobre la ecología microbiana acuática.

Referencias bibliográficas

  • Amaral-Zettler L.A., Zettler E.R., Mincer T.J. 2020. Ecology of the plastisphere. Nat. Rev. Microbiol.18: 139-151. https://doi.org/10.1038/s41579-019-0308-0PMid:31937947
  • Astudillo-García C., Hermans S.M., Stevenson B., Buckley H.L., Lear G. 2019. Microbial assemblages and bioindicators as proxies for ecosystem health status: potential and limitations. Appl. Microbiol. Biot. 103: 6407-6421. https://doi.org/10.1007/s00253-019-09963-0PMid:31243501
  • Bertagnolli A.D., Stewart F.J. 2018. Microbial niches in marine oxygen minimum zones. Nat. Rev. Microbiol. 16: 723-729.https://doi.org/10.1038/s41579-018-0087-zPMid:30250271
  • Biller S.J., Berube P.M., Dooley K., et al. 2018. Data descriptor: Marine microbial metagenomes sampled across space and time. Sci. Data 5: 180176. https://doi.org/10.1038/sdata.2018.176PMid:30179232 PMCid:PMC6122167
  • Boavida M.J. 2012. It all started with Margalef's paper of 1951. Limnetica 31: 187-192.https://doi.org/10.23818/limn.31.17
  • Borrero-Santiago A.R., DelValls T.A., Riba I. 2016. Carbon Capture and Storage (CCS): Risk assessment focused on marine bacteria. Ecotoxicol. Environ. Saf. 131: 157-163. https://doi.org/10.1016/j.ecoenv.2016.04.020PMid:27107627
  • Botta-Dukát Z. 2005. Rao's quadratic entropy as a measure of functional diversity based on multiple traits. J. Veg. Sci. 16: 533-540. https://doi.org/10.1111/j.1654-1103.2005.tb02393.x
  • Boyd P.W., Collins S., Dupont S., et al. 2018. Experimental strategies to assess the biological ramifications of multiple drivers of global ocean change-A review. Glob. Change Biol. 24: 2239-2261. https://doi.org/10.1111/gcb.14102PMid:29476630
  • Brown J.H., Gillooly J.F., Allen A.P., et al. 2004. Toward a metabolic theory of ecology. Ecology 85: 1771-1789. https://doi.org/10.1890/03-9000
  • Defining the scientific method. 2009. Nat. Methods 6: 237. https://doi.org/10.1038/nmeth0409-237PMid:19340960
  • Dlugokencky E., Tans P. 2020. Global Monitoring Laboratory-Carbon Cycle Greenhouse Gases. Retrieved July 6, 2020, from www.esrl.noaa.gov/gmd/ccgg/trends.
  • Dyhrman S.T., Ammerman J.W., Van Mooy B.A.S. 2007. Microbes and the marine phosphorus cycle. Oceanography 20: 110-116. https://doi.org/10.5670/oceanog.2007.54
  • Ehrlich P.R., Ehrlich A.H. 1981. Extinction: the causes and consequences of the disappearance of species. New York: Random House.
  • Emamalipour M., Seidi K., Vahed S. Z., et al. 2020. Horizontal gene transfer: from evolutionary flexibility to disease progression. Front. Cell Develop. Biol. 8. https://doi.org/10.3389/fcell.2020.00229PMid:32509768 PMCid:PMC7248198
  • Fastner J., Rucker J., Stuken A., et al. 2007.Occurrence of the cyanobacterial toxin cylindrospermopsin in northeast Germany. Environ. Toxicol. 22: 26-32. https://doi.org/10.1002/tox.20230PMid:17295278
  • Fontana S., Rasmann S., de Bello F., et al. 2021. Reconciling trait-based perspectives along a trait-integration continuum. Ecology 102(10): e03472. https://doi.org/10.1002/ecy.3472PMid:34260747
  • Fuente, M.d.L., Miranda, C.D., Jopia, P., et al. 2015. Growth inhibition of bacterial fish pathogens and quorum-sensing blocking by bacteria recovered from Chilean salmonid farms. J. Aquat. Anim. Health 27: 112-122. https://doi.org/10.1080/08997659.2014.1001534PMid:26000731
  • Fuhrman J.A., Hagstrom K. 2008. Bacterial and Archaeal Community Structure and its Patterns. In: Microbial Ecology of the Oceans (pp. 45-90). Hoboken, NJ, USA: John Wiley and Sons, Inc. https://doi.org/10.1002/9780470281840.ch3
  • Gattuso J.P., Hansson L. 2011. Ocean acidification: background and history. In: Ocean Acidification, Oxford Univ. Press, Inc. USA. https://doi.org/10.1093/oso/9780199591091.003.0006
  • Ghyoot C., Gypens N., Flynn K.J., Lancelot C. 2015. Modelling alkaline phosphatase activity in microalgae under orthophosphate limitation: the case of Phaeocystis globosa. J. Plankton Res. 37: 869-855. https://doi.org/10.1093/plankt/fbv062
  • González-Ortegón E.; Moreno-Andrés J. 2021. Anthropogenic Modifications to Estuaries Facilitate the Invasion of Non-Native Species. Processes 9: 740. https://doi.org/10.3390/pr9050740
  • Goodrich J.K., Waters J.L., Poole A.C., et al. 2014. Human genetics shape the gut microbiome. Cell 159: 789-799. https://doi.org/10.1016/j.cell.2014.09.053PMid:25417156 PMCid:PMC4255478
  • Goswami M., Bhattacharyya P., Mukherjee I., Tribedi P. 2017. Functional diversity: an important measure of ecosystem functioning. Adv. Microbiol. 7: 82-93. https://doi.org/10.4236/aim.2017.71007
  • Gruber N. 2011. Warming up, turning sour, losing breath: ocean biogeochemistry under global change. Philos. Trans. R. Soc. A 369: 1980-1996. https://doi.org/10.1098/rsta.2011.0003PMid:21502171
  • Guo X., Wang J. 2019. The chemical behaviors of microplastics in marine environment: A review. Mar. Poll. Bull. 142: 1-14. https://doi.org/10.1016/j.marpolbul.2019.03.019PMid:31232281
  • Heidelberg K.B., O'Neil K.L., Bythell J.C., Sebens K.P. 2010. Vertical distribution and diel patterns of zooplankton abundance and biomass at Conch Reef, Florida Keys (USA). J. Plankton Res. 32(1): 75-91. https://doi.org/10.1093/plankt/fbp101PMid:20046854 PMCid:PMC2787388
  • Hultman J., Waldrop M.P., Mackelprang R., et al. 2015. Multi-omics of permafrost, active layer, and thermokarst bog soil microbiomes. Nature. 521: 208-212. https://doi.org/10.1038/nature14238PMid:25739499
  • Jing H., Xia X., Suzuki K., Liu H. 2013.Vertical profiles of bacteria in the tropical and subarctic oceans revealed by pyrosequencing. PLoS ONE 8: e79423. https://doi.org/10.1371/journal.pone.0079423PMid:24236132 PMCid:PMC3827353
  • Jones S.J., Southward A.J., Wethey D.S. 2012. Climate change and historical biogeography of the barnacle. Global Ecol. Biogeogr. 21: 716-724. https://doi.org/10.1111/j.1466-8238.2011.00721.x
  • Lawton J. H. 1994. What do species do in ecosystems? Oikos 71: 367. https://doi.org/10.2307/3545824
  • Lawton J. H. 1999. Are there general laws in ecology? Oikos 84: 177-192. https://doi.org/10.2307/3546712
  • Lepš J. 2005. Diversity and ecosystem function. Veg. Ecol. 199-237.
  • Letscher R.T., Moore J.K. 2015. Preferential remineralization of dissolved organic phosphorus and non-Redfield DOM dynamics in the global ocean: Impacts on marine productivity, nitrogen fixation, and carbon export. Global Biogeochem. Cy. 29: 325-340.https://doi.org/10.1002/2014GB004904
  • Levine J.M., Adler P.B., Yelenik S.G. 2004. A meta-analysis of biotic resistance to exotic plant invasions. Ecol. Lett. 7: 975-989. https://doi.org/10.1111/j.1461-0248.2004.00657.x
  • Locey K.J. Lennon J.T. 2016. Scaling laws predict global microbial diversity. Proc. Nat. Acad. Sci. USA 113: 5970-5975. https://doi.org/10.1073/pnas.1521291113PMid:27140646 PMCid:PMC4889364
  • Logares R., Haverkamp T.H.A., Kumar S., et al. 2012. Environmental microbiology through the lens of high-throughput DNA sequencing: Synopsis of current platforms and bioinformatics approaches. J. Microbiol. Met. 91: 106-113. https://doi.org/10.1016/j.mimet.2012.07.017PMid:22849829
  • Margalef R. 1950. Rôle des entomostracés dans la régéneration des phosphates, internationale vereinigung für theoretische und angewandte. Limnologie: Verhandlungen. 11: 246-247. https://doi.org/10.1080/03680770.1950.11895232
  • Margalef R. 1951. Diversidad de especies en les communidades naturales. Publ. Inst. Biol. Apl. Barcelona 6: 59-72.
  • Margalef R. 1957. La teoría de la información en Ecología. Mem. Real Acad. Cien. Art. Barcelona 32: 373-436.
  • Margalef R. 1958. Information theory in ecology. General Systems: Yearbook of the Society for General Systems Research 3: 36-71.
  • Margalef R. 1963. On certain unifying principles in ecology. Amer. Nat. 97(897): 357-374. https://doi.org/10.1086/282286
  • Margalef R. 1968. Perspectives in ecological theory. University of Chicago Press. 111 pp.
  • Margalef R. 1975. Diversity, stability and maturity in natural ecosystems. In: Unifying Concepts in Ecology. Springer, Netherlands, pp. 151-160. https://doi.org/10.1007/978-94-010-1954-5_12
  • Margalef R. 1978. Life-forms of phytoplankton. Oceanol. Acta 1: 493-509.
  • Margalef R. 1985. Ecosystems: diversity and connectivity as measurable components of their complication. In: The Science & Praxis of Complexity. United Nations University (UNU), Tokyo, GLDB-2/UNUP-560.
  • Margalef R. 1991. Teoría de los sistemas ecológicos. Edicions Universitat Barcelona.
  • Margalef R. 1992. Oblik Biosfer (A View of the Biosphere). Moscow: Russian Academy of Sciences, Institute of Oceanology.
  • Margalef R. 1997. Our biosphere. In: O. Kinne (ed.), Excellence in Ecology, 10. Ecology Institute, Oldendrof/Luhe, 176 pp.
  • Margalef R. 1998. Elements limitants, explotabilitat i diversitat. Homenatge a Bolòs i al fòsfor. Acta Bot. Barcino. 45: 633-643. Retrieved from. https://raco.cat/index.php/ActaBotanica/article/view/59590
  • Margalef R. 2000a. El marco ecológico para iluminar la sociedad actual. In: Naredo J.M. and Parra F. (eds), Economía, Ecología y Sostenibilidad en la sociedad actual. Siglo XXI, Madrid, pp. 51-66.
  • Margalef R. 2000b. Organització de la biosfera i reflexions sobre el present i el futur de la nostra espècie i de la ciència ecològica. Treb. Soc. Cat. Biol. 50: 47-59. Retrieved from. https://raco.cat/index.php/TreballsSCBiologia/article/view/15701
  • Margalef R., Estrada M., Blasco D. 1979. Functional morphology of organisms involved in red tides, as adapted to decaying turbulence. In: Taylor, D., Seliger, H. (eds), Toxic Dinoflagellate Blooms. Elsevier, New York pp. 89-94.
  • Mestre M., Höfer J., Sala M.M., Gasol J.M. 2020. Seasonal variation of bacterial diversity along the marine particulate matter continuum. Front. Microbiol. 11: 1590. https://doi.org/10.3389/fmicb.2020.01590PMid:32793139 PMCid:PMC7385255
  • Morris E.K., Caruso T., Buscot F., et al. 2014. Choosing and using diversity indices: Insights for ecological applications from the German Biodiversity Exploratories. Ecol. Evol. 4: 3514-3524. https://doi.org/10.1002/ece3.1155PMid:25478144 PMCid:PMC4224527
  • Moseman S.M., Zhang R., Qian P.Y., Levin L.A. 2009. Diversity and functional responses of nitrogen-fixing microbes to three wetland invasions. Biol. Invasions 11: 225-239. https://doi.org/10.1007/s10530-008-9227-0
  • Ortiz-Álvarez R., Fierer N., De Los Ríos A., Casamayor E.O., Barberán A. 2018. Consistent changes in the taxonomic structure and functional attributes of bacterial communities during primary succession. ISME J. 12: 1658-1667. https://doi.org/10.1038/s41396-018-0076-2PMid:29463893 PMCid:PMC6018800
  • Pettorelli N., Schulte to Bühne H., Tulloch A., et al. 2018. Satellite remote sensing of ecosystem functions: opportunities, challenges and way forward. Remote Sens. Ecol. Cons. 4: 71-93. https://doi.org/10.1002/rse2.59
  • Pielou, E. C. 1966. The measurement of diversity in different types of biological collections. J. Theor. Biol. 13: 131-144. https://doi.org/10.1016/0022-5193(66)90013-0
  • Pinhassi J., Hagström Å. 2000. Seasonal succession in marine bacterioplankton. Aquat. Microb. Ecol. 21: 245-256.https://doi.org/10.3354/ame021245
  • Polaske N.W., Kelly B.D., Ashworth-Sharpe J., Bieniarz C. 2016. Quinone methide signal amplification: covalent reporter labeling of cancer epitopes using alkaline phosphatase substrates. Bioconjug. Chem. 27: 660-666. https://doi.org/10.1021/acs.bioconjchem.5b00652PMid:26731201
  • Prosser J.I. 2010.Replicate or lie. Env. Microbiol. 12: 1806-1810. https://doi.org/10.1111/j.1462-2920.2010.02201.xPMid:20438583
  • Pylro V.S., Roesch L.F.W., Morais D.K., et al. 2014. Data analysis for 16S microbial profiling from different benchtop sequencing platforms. J. Microbiol. Meth. 107: 30-37. https://doi.org/10.1016/j.mimet.2014.08.018PMid:25193439
  • Rao C.R. 1982. Diversity and dissimilarity coefficients: a unified approach. Theor. Pop. Biol. 21: 24-43. https://doi.org/10.1016/0040-5809(82)90004-1
  • Rosenzweig C., Parry M.L. 1994. Potential impact of climate change on world food supply. Nature 367: 133-138. https://doi.org/10.1038/367133a0
  • Sánchez-Quinto A., Falcón L.I. 2019. Metagenome of Acropora palmata coral rubble: Potential metabolic pathways and diversity in the reef ecosystem. PLoS ONE 14: e0220117. https://doi.org/10.1371/journal.pone.0220117PMid:31394568 PMCid:PMC6687439
  • Schroeder P.J., Jenkins D.G. 2018. How robust are popular beta diversity indices to sampling error? Ecosphere 9: e02100. https://doi.org/10.1002/ecs2.2100
  • Sebastian M., Ammerman J.W. 2009. The alkaline phosphatase PhoX is more widely distributed in marine bacteria than the classical PhoA. ISME J. 3: 563-572. https://doi.org/10.1038/ismej.2009.10PMid:19212430
  • Shade A. 2017. Diversity is the question, not the answer. ISME J. 11: 1-6. https://doi.org/10.1038/ismej.2016.118PMid:27636395 PMCid:PMC5421358
  • Shannon C.E., Weaver W. 1949. The mathematical theory of communication. The University of Illinois Press, Urbana.
  • Simpson E.H. 1949. Measurement of diversity. Nature 163: 688. https://doi.org/10.1038/163688a0
  • Sherwin W.B., Prat i Fornells N. 2019. The Introduction of Entropy and Information Methods to Ecology by Ramon Margalef. Entropy 21: 794. https://doi.org/10.3390/e21080794PMid:33267507 PMCid:PMC7515323
  • Terradas J. 2015. El pensamiento evolutivo de Margalef. Ecosistemas 24: 104-109.
  • Thomas M.K., Fontana S., Reyes M., Kehoe M., Pomati F. 2018. The predictability of a lake phytoplankton community, over time-scales of hours to years. Ecol. Lett. 21: 619-628. https://doi.org/10.1111/ele.12927PMid:29527797
  • Tuomisto H. 2010. A diversity of beta diversities: Straightening up a concept gone awry. Part 2. Quantifying beta diversity and related phenomena. Ecography 33: 23-45. https://doi.org/10.1111/j.1600-0587.2009.06148.x
  • Valdespino-Castillo P.M., Alcántara-Hernández R.J., Alcocer J., et al. 2014. Alkaline phosphatases in microbialites and bacterioplankton from Alchichica soda lake, Mexico. FEMS Microbiol. Ecol. 90: 504-519. https://doi.org/10.1111/1574-6941.12411PMid:25112496
  • Vellend M. 2016. The theory of ecological communities. In: Monographs in population biology. Princeton University Press. https://www.jstor.org/stable/j.ctt1kt82jg
  • Villamaña M., Marañón E., Cermeño P., Estrada M., Fernández-Castro B., Figueiras F. G., Latasa M., Otero-Ferrer J. L., Reguera B., Mouriño-Carballido B. 2019. The role of mixing in controlling resource availability and phytoplankton community composition. Prog. Oceanogr. 178: 102181. https://doi.org/10.1016/j.pocean.2019.102181
  • Vitorino L.C., Bessa L.A. 2018. Microbial diversity: the gap between the estimated and the known. Diversity 10: 46. https://doi.org/10.3390/d10020046
  • Wyatt T. 2014. Margalef's mandala and phytoplankton bloom strategies. Deep-Sea Res. Pt. II 101: 32-49.https://doi.org/10.1016/j.dsr2.2012.12.006
  • Wyatt T., Carlton J.T. 2002. Phytoplankton introductions in European coastal waters: why are so few invasions reported? In: Briand F. (ed), Alien Marine Organisms Introduced by Ships in the Mediterranean and Black Seas - Commission Internationale pour l'Exploration Scientifique de la Mer Mediterranee. 20: 41-46.
  • Young J.N., Rickaby R.E.M., Kapralov M., Filatov D.A. 2012. Adaptive signals in algal Rubisco reveal a history of ancient atmospheric carbon dioxide. Philos. Trans. R. Soc. B 367: 483-492.https://doi.org/10.1098/rstb.2011.0145PMid:22232761 PMCid:PMC3248704