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Gayana (Concepción)

versión impresa ISSN 0717-652Xversión On-line ISSN 0717-6538

Gayana (Concepc.) v.70  supl.1 Concepción oct. 2006 

Suplemento Gayana 70: 68-72, 2006


Living in the oxygen minimum zone: A metabolic perspective

Viviendo en la zona de mínimo de oxígeno: Una perspectiva metabólica

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

2 Department of Oceanography, Faculty of Natural and Oceanographica Sciences, University of Concepcion, Concepción-Chile


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.


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 Claves: 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).

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-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 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 sp., 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.

Microplankton 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 (<100 mm), and their association with oxygen concentration and microplanktonic biomass in the OMZ and adjacent areas of the water column. Our results demonstrate significant potential enzymatic activity of catabolic pathways in the OMZ, implying that this portion of the water column is biogeochemically active. Malate dehydrogenase (MDH) had the highest oxidizing activity of the batch of catabolic enzymatic activities assayed, including potential pyruvate oxidoreductases activity, the electron transport system, and dissimilatory nitrate reductase. MDH correlated significantly with almost all the enzymes analyzed within and above the oxygen minimum zone, and also with oxygen concentration and microplankton biomass in the water column, especially in the OMZ off northern Chile. We propose the use of MDH activity as an indicator of microbial activity for microplanktonic communities that live in the whole water column of the HCS (González et al., submitted a).

On the other hand, experiments were conducted to compare the effect of four sources of dissolved organic carbon (DOC: glucose, glycine, leucine, and oxaloacetate) on microbial biomass production (ATP-P) and the potential enzymatic activities involved in catabolic pathways under oxic and suboxic conditions (González et al., submitted b). Results show significant differences in the production of ATP-P induced by the different substrates used. The induction of ATP-P production is enhanced differentially in the following order: glucose <oxaloacetate <glycine <leucine. Nevertheless, for single substrates, no significant differences were found between incubation under oxic and suboxic conditions except in the case of leucine, for which induction of ATP-P synthesis was higher under suboxic than oxic conditions. All substrates used showed greater potential ATP-P production under suboxic than oxic conditions. These findings suggest that the microbial community inhabiting the OMZ has the same or higher potential growth than the community inhabiting more oxygenated strata of the water column. The catabolic demand of the microplankton cells in the OMZ correspond to 7.36 ng C day-1 pgATP-1.

The allometry of anaerobic metabolism in the HCS

The relationship between body size and anaerobic metabolism in species and communities inhabiting OMZ's remains scarcely known. LDH activities were determined at the species level in zooplankton (300-1000 µm) and benthic (>500 µm) assemblages, and in size fractions of microplankton (<100 µm) and netplankton (65-1000 µm) assemblages (González et al., submitted c). The profile of LDH activities shows high MDH activity as a common pattern for all assemblages analyzed. In the zooplankton assemblage, high LDH activity was observed and, in the benthic assemblage, high OPDH activities were found. In microplankton and netplankton assemblages, MDH presented the highest activity. Across the community, a common significant allometric relationship (log-log scale) was found for specific LDH activity (single-species and size-fraction levels). This LDH allometric relationship always had a positive slope presenting a wide range of intercepts without a unified curve as is observed for the aerobic metabolism. The strong relationship found between LDH and MDH activities across the analyzed species assemblages suggests that the LDH/MDH ratio is a key scaling factor for the anaerobic catabolism (González et al., submitted b, c)

At the species level a positive allometric relationship was found between body size and the specific activity of ALPDH, STRDH, and maximum pyruvate oxidoreductase specific activity in polychaetes (González & Quiñones 2000). We have also found positive allometric scaling of anaerobic metabolism in E. mucronata (González & Quiñones 2002), and in the deep benthic polychaete Hyalinoecia artifex.

Furthermore, we have analyzed the distribution of metabolism (aerobic and anaerobic) and biomass by size in the benthos at the community level of organization. This is the first time that empirical aerobic and anaerobic metabolic size-spectra are constructed in benthic communities worldwide. Four oceanographic stations located on a transect from the inner Bay of Concepción to the mid-continental shelf were sampled. Biomass was estimated as total ATP concentration and the aerobic metabolic activity was assessed evaluating the ETS and CS activity. The activity of LDH and MDH was estimated as indicators of anaerobic metabolism. Biomass and aerobic metabolism diminishes with the increment of body size at the community level of organization. The negative slopes of the normalized biomass spectra as well as those of the metabolic spectra, demonstrate the importance at the community level of organization played by the smaller organisms both from the standpoint of biomass as well as aerobic metabolism. Regarding the activity of MDH and LDH, the values of the slopes of the normalized spectra were -0,872 and -0,917 respectively, indicating that anaerobic activity increases slightly with body size at the community level of organization.

Archaea abundance, and secondary production in the OMZ

We have quantified Archaea in the water column, including the OMZ and the benthic boundary layer (BBL) using dot-blot techniques, and PCR. Archaeal abundance was usually greater in the deeper layer (>50 m), with contributions reaching up to ~ 90 % of the prokaryote rRNA and decreasing towards the surface. Our results indicate that Archaea constitute an important fraction of the marine bacterioplankton in the water column of the HCS, especially in the OMZ (Quiñones et al., submitted). Molecular analysis shows a strong presence of 16S rRNA genes of Crenarchaeota group I. After developing a proper methodology using 14C-leucine and N1-guanyl-1, 7-diaminoheptane (GC7), an efficient inhibitor of archaeal and eukaryote cell growth, a time series of Archaea secondary production (ASP) in the benthic boundary layer was conducted from November 2002 to June 2004 (Levipán et al., submitted a). ASP was variable through the year presenting values between 0.00071 to 0.23 mg C L-1 h-1. In general, ASP ranged between 20 and 85% of the total prokaryote production. It is important to note that the biogeochemical role of Archaea is scarcely known globe-wise and that our ASP estimations are among the very few first direct ones (Levipán et al., submitted a). On the other hand, the distribution and abundance of methane-producing Archaea (MPA) were studied in the water column of the upwelling area off Concepción (~ 36° S), central Chile. The methanogens were detected in the water column mostly during an active upwelling period (austral spring-summer), representing ~10 % of the total prokaryote rRNA in the OMZ. Enrichment experiments with seawater samples taken from the OMZ showed that some of these Archaea remain viable in the planktonic environment, although not essentially associated to large fecal pellets or some type of compact macroaggregate. The results suggest that the MPA in the water column come mostly from the ocean floor and that an important fraction of these correspond to psychrophilic non-methylotrophic varieties (Levipán et al., submitted b).


This research was funded by the FONDAP-COPAS Center (CONICYT, Chile)


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