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TheAzolla-Anabaena association: Historical perspective, symbiosis and energy metabolism

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Abstract

The heterosporous water-fern genusAzolla is one of the few symbioses with a cyanobacterium in the genusAnabaena. TheAzolla-Anabaena association includes six extant speciesof Azolla, which are widely distributed in relatively placid tropical and/or temperate freshwater environments.

The earliest mention of the plant seems to be in an ancient Chinese dictionary that appeared about 2000 years ago.Azolla was used in about the 11th century in Vietnam. By 1980 renewed interest in this symbiotic association was shown by the demand for a less fossil energy-dependent agricultural technology. The importation of a variety ofA. filiculoides may have been a most significant breakthrough for the improvementof Azolla cultivation in China. The history of research may be divided into three periods and a new biotechnological stageof Azolla research has recently begun.

Each mature dorsal leaf lobe has an ellipsoid cavity which containsAnabaena azollae throughout its development. HeterocystousA. azollae from sixAzolla species share identical and highly specific antigens.Azolla and its endophyte exhibit a coordinated pattern of differentiation and development. Epidermal hair cells of the host are probably interactive with the symbiont. The interior surface of a mature leaf cavity is lined with an envelope and covered by a mucilaginous layer.A. azollae shares the cavity with small populations of the bacteriaPseudomonas andAzotobacter. Endophyte-freeAzolla may rarely occur in nature and can be generated by aseptic techniques.Anabaena azollae can be isolated fromAzolla fronds by gentle pressure and by enzymatic digestion. The free living cultures derived from theAnabaena so obtained differ in some respects, however, from the freshly extracted symbiont, and might better be called the presumptive isolate.

BothAzolla andAnabaena contain specific photosynthetic pigments. The optimum conditions for photosynthesis have been measured.Azolla is a C3 plant and has high net photosynthesis. PSII activity in the symbiont is low. Nitrogenase is localized in the heterocysts of the symbiont and has some advantages compared with free-living cyanobacteria. SymbioticA. azollae has a high frequency of heterocysts. Unidirectional hydrogenase occurs in the symbiont and recycles electrons and ATP. Simultaneous measurements of N2 fixation and photosynthesis show the dependence of nitrogenase on photosynthetically captured radiation for energy by an indirect dependence on CO2 fixation. The host contains most of the total GS and GDH activities, and the symbiont excretes a substantial portion of its newly fixed nitrogen as ammonium. The two partners in the association exhibit a comparable developmental gradient and a mechanism of cooperative integration for their energy metabolism, thus improving the efficiency of solar energy conversion and presenting a unique model for biotechnology.

Sumario

El género acuáticoAzolla es una de las pocas plantas simbióticas cianobacterianas, dentro del géneroAnabaena. El géneroAzolla-Anabaena incluye seis especies bastante bien conocidas, ampliamente distribuidas en zonas tropicales apacibles y en ambientes de aguas templadas.

El data mas antiguo que se tiene de ésta planta parece orginarse de un diccionario chino hace unos 2000 años.Azolla ya se utilizaba en Vietnam por el siglo XI. Para el año 1980 esta asociación simbiótica habia despertado un gran interés, estimulado por la necesidad de reducir la dependencia energética del petróleo en el sector agrario.

La introducción de una variedad deA. filiculoides parece haber sido uno de los pasos mas decisivos en el mejoramiento del cultivo de ésta planta en China. Historicamente el estudio científico de laAzolla puede dividirse en tres fases principales, junto con una reciente etapa de investigatión biotecnológica.

La parte interior de la hoja madura tiene una cavidad elíptica que contieneAnabaena azollae a lo largo de su desarrollo.A. azollae orginaria de seis especies diferentes deAzolla, comparten antigenos idénicos y altamente especializados. La actividad endófica de laAzolla exibe un cierto patron de coordinación y desarrollo. Los pelillos epidérmicos celulares del tronquillo son probablemente interactivos con la simbioses. La parte interior elliptica de la hoja madura está cubierta de una tela mucosa.A. azollae comparte esta cabidad con una población pequeña de bacteriasPseudomonas yAzotobacter. “Endophyte-free”Azolla raramente se da en la naturaleza, pudiendo ser generada por medio de técnicas asépticas. La separación deA. azollae puede otenerse presionando suavemente éstas o por medio de digestión enzimática, y se ha demostrado por medios inmunológicos y patrones de hibridización que estos no están estrechamente relacionados a la simbiosis de la planta.

TantoAzolla comoAnabaena contienen ciertos pigmentos fotosintéticos específicos. Las condiciones óptimas fotosintéticas de laAzolla han sido ya calculadas.Azolla es una planta C3 con alta capacidad fotosintética. La actividad de PSII en la simbiosis es baja. E1 nitrógeno se localiza en areas heterocistas simbióticas, ofreciendo ciertas ventajas comparadas con cianobacteria libre. La simbiosis deA. azollae posee una alta frecuencia heterocista. La hidrogenizacion occurre en la simbiosis, reciclando electrones y ATP. Trabajos realizados simultaneamente para medir la fijación de nitrógeno y de fotosíntesis, muestran la dependencia del nitrógeno en la radiación capturada fotosinteticamente por la energia y una dependencia indirecta en cuanto a la fijación de CO2. La parte troncular contiente la mayor parte de las actividades activas de GS y GDH, mientras que la simbiosis excreta una parte substancial de su nitrógeno nuevamente fijado como amonio. Este acoplamiento exibe un gradiente de desarrollo y un mecanismo de integración conjunto y de cooperación substancial en su metabolismo energético, a fin de mejorar su eficacia en la conversión de energía solar, por lo cual presenta un modelo único para la biotecnología.

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  1. Ding-Ji Shi

    Present address: Institute of Botany, Academia Sinica, 100044, Beijing, China

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Shi, DJ., Hall, D.O. TheAzolla-Anabaena association: Historical perspective, symbiosis and energy metabolism. Bot. Rev 54, 353–386 (1988). https://doi.org/10.1007/BF02858416

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