Suplemento Gayana 70, 2006
ISSN 0717-652X
LIVING IN THE OXYGEN MINIMUM ZONE: A METABOLIC PERSPECTIVE VIVIENDO EN LA ZONA DE MINIMO DE OXIGENO: UNA PERSPECTIVA METABOLICA Renato A. Quiñones1,2 , Rodrigo R. González1,2 , Héctor Levipan1 , Gerdhard Jessen1,2 & Marcelo H. Gutiérrez2 1
Center for Oceanographic Research in the Eastern South Pacific (FONDAP-COPAS), University of Concepcion, P.O. Box 160-C, Concepción, Chile
[email protected] 2 Department of Oceanography, Faculty of Natural and Oceanographica Sciences, University of Concepcion, Concepción-Chile ABSTRACT Respiration is a key variable to understand the flux of energy and matter in any ecosystem. In fact, ecosystem respiration is a critical component of the carbon cycle and might be important in regulating biosphere response to global climate change. Respiration is the basic process used by the biota to yield energy from the degradation of organic matter for their survival needs, its measurement provides an estimate of the minimum energy needed by the organism. Accordingly, the total respiration of an aquatic community can be equated to the minimum energy needed to maintain its organized living structure and function. Despite its importance, community respiration has been a process scarcely studied in the ocean and only during the 90’s has become more relevant. In fact, whereas aerobic metabolism has been scarcely studied in ocean systems, anaerobic metabolism, especially at the community level of organization, has been largely neglected. KEYWORDS: Anaerobic metabolism, respiration, oxygen minimum zone, Humboldt Current system. RESUMEN La respiración es la variable clave para comprender el flujo de energía y materia en cualquier ecosistema. De hecho, la respiración del ecosistema es un componente critico del ciclo del carbono y podría ser importante en la regulación de la respuesta de la biosfera al cambio climático. La respiración es el proceso básico usado por la biota en la obtención de energía de la degradación de la materia orgánica para satisfacer sus necesidades de supervivencia; su medición entrega un estimado de la cantidad mínima de energía que necesita el organismo. De acuerdo con esto, la respiración total de la comunidad acuática puede ser igualada a la energía mínima que necesita para mantener su estructura vital y su funcionamiento. A pesar de su importancia, la respiración comunitaria es un proceso escasamente estudiado en el océano y solo a partir de los 90’s ha pasado a ser relevante. De hecho, mientras el metabolismo aeróbico ha sido escasamente estudiado en los sistemas oceánicos, el metabolismo anaeróbico, especialmente al nivel de organización de la comunidad, ha sido mayoritariamente descuidado. PALABRAS CLAVE: Metabolismo anaeróbico, respiración, zona de mínimo oxígeno, Sistema de Corrientes Humboldt.
The presence of the subsurface OMZ in extensive areas of the HCS has important effects on the metabolism of the organisms inhabiting this environment. Species deal with the hypoxic and anoxic environments by relying on biochemical, physiological and behavioral adaptations, which seem to be critical in the HCS where oxygen levels lower than 136.0 mmol O2 m-3 act as a physical barrier for aerobic respiration in the water column (Eissler & Quiñones 1999).
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Our laboratory has been studying metabolism in the HCS, both in the benthic and pelagic realms, since early 90’s. We have analyzed respiration at different levels of organization (individuals, communities) and using both taxonomic and ataxonomic approaches. In the latter case we have utilized functional groupings and size structured approaches. It is important to note that whereas the allometry of aerobic metabolism is well known (e.g., Peters 1983, Marquez et al., 2005), the relationship between body-
Gayana 70 (Suplemento): Respiration in the OMZ 20-25, 2006
size and anaerobic metabolism remains scarcely documented. Our studies have comprised microorganisms, invertebrates and vertebrates. In summary, our research shows that (i) respiration is a key process to understand the fluxes of energy an matter in the OMZ of the HCS, (ii) the microbial community in the OMZ is very active from a biogeochemical standpoint, (iii) the activity of malate dehydrogenase can be used as an estimator of total metabolic activity in the OMZ, (iv) Archaea plays a fundamental role among the prokaryotes living in the OMZ, and (v) there are regularities in the distribution of aerobic and anaerobic metabolism by size at the community level of organization in the OMZ. BIOCHEMICAL ADAPTATIONS TO
ENVIRONMENTAL LOW
OXYGEN CONDITIONS
Our results show that the kinetic parameters of the enzymes as well as the number of enzymatic pathways involved in anerobic metabolism present in each species are critical for their behavioral responses to low oxygen conditions. The euphausiid Euphausia mucronata and the copepod Calanus chilensis are key species in the HCS from a trophodynamic and an abundance standpoint. E. mucronata is able to have a daily vertical migration through the OMZ, whereas C . chilensis, inhabiting the oxygenated waters over the OMZ, is not. Taking advantage of the contrasting vertical migratory patterns of these key species, we compared their anaerobic enzymatic characteristics and activities (Gonzalez y Quiñones 2002). Organisms capable of daily vertical migration though the OMZ are expected to reflect, to some extent, an adaptation to the hypoxic environment in their energy metabolisms and a reliance on biochemical as well as physiological mechanisms involved in anaerobic metabolism. Indeed, the specific lactate dehydrogenase (LDH) activity in E. mucronata was two orders of magnitude higher than that of C . chilensis, consistent with E. mucronata’s ability to conduct daily vertical migrations through the oxygen minimum layer. In contrast, C. chilensis is restricted to inhabiting oxygenated waters over the oxygen minimum layer without carrying out daily vertical migrations across it. Polychaete assemblages cohabit on the shelf with an extensively distributed prokaryotic community made up of giant filamentous sulfur bacteria (mainly Thioploca sp.) (see Gallardo 1985). We characterized
ISSN 0717-652X
the pyruvate oxidoreductases enzymes involved in the biochemical adaptation of these benthic polychaetes (González & Quiñones 2000). Nine polychaetes species (Paraprionospio pinnata, Nephtys ferruginea, Glycera americana, Haploscoloplos s p ., Lumbrineris composita , Sigambra bassi, Aricidea pigmentata, Cossura chilensis, and Pectinaria chilensis) were assayed for LDH, octopine dehydrogenase (OPDH), strombine dehydrogenase (STRDH) and alanopine dehydrogenase (ALPDH). Each species had a characteristic number of the pyruvate oxidoreductases assayed ranging from four in Paraprionospio pinnata to one in Pectinaria chilensis. The pyruvate saturation curves obtained for the enzymes from all species analyzed, except L. composita, suggest that NADH can be oxidized at different rates depending on the amino acid used in the reaction with pyruvate. Our results indicate that organisms having more that one pyruvate oxidoreductase present a greater metabolic capacity to cope with functional and environmental hypoxia because these enzymes would better regulate the pyruvate consumption rate during the transition period. Thus, the dominance of P. pinnata in the study area and its worldwide distribution is consistent with its higher number of pyruvate oxidoreductases with different pyruvate consumption rates involved in anaerobic metabolism. M ICROPLANKTON ANAEROBIC METABOLISM We have characterized, for the first time in the HCS (González & Quiñones, submitted), the potential enzymatic activities involved in the aerobic and anaerobic energy production pathways of microplanktonic organisms (
