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Gayana (Concepción)

Print version ISSN 0717-652XOn-line version ISSN 0717-6538

Gayana (Concepc.) vol.70  suppl.1 Concepción Oct. 2006

http://dx.doi.org/10.4067/S0717-65382006000300018 

Suplemento Gayana 70: 83-86, 2006


Microbial communities and their biogeochemical role in the water column of the oxygen minimum zone in the eastern South Pacific

Comunidades microbianas y su rol biogeoquImico en la columna de agua de la zona de mínimo de oxIgeno en el PacIfico Sudoriental

Osvaldo Ulloa1, Lucy Belmar1, Laura Farías1, Maribel Castro-González1,2, Alexander Galán1, Paris Lavín1,3, Verónica Molina1, Salvador Ramírez, Francisco Santibáñez1 & Heike Stevens1

1 Laboratory of Oceanographic and Climate Processes (PROFC), Department of Oceanography & Center for Oceanographic Research in the Eastern South Pacific (FONDAP-COPAS), University of Concepcion, P.O. Box 160-C, Concepción, Chile, oulloa@profc.udec.cl

2 Department of Biology, University of Tolima, Colombia.

3 Department of Botany, University of Concepción, Concepción, Chile


ABSTRACT

In recent years, our group has been studying the microbial communities of the water column associated with the oxygen minimum zone (OMZ) off northern Chile and Peru, trying to understand who the main players are in the OMZ biogeochemical cycles and which metabolic strategies they are using. For that, we are combining flow cytometry, molecular techniques and biogeochemical approaches. Most of our work, so far, has focused on microbes capable of doing oxygenic photosynthesis, such as the cyanobacteria, and those involved in the nitrogen cycle, such as the denitrifying, nitrifying and anammox bacteria. We have also started to look at the more general microbial abundance and diversity. In each case, we are finding that the OMZ holds distinct microbial communities, either from a phylogenetic or a functional perspective. In this presentation we will give a summary of our main results.

Keywords: Oxygen minimum zone, microbial diversity, nitrogen cycle.


RESUMEN

El los último años, nuestro grupo ha estado estudiando las comunidades microbianas de la columna de agua asociada a la zona de mínima de oxígeno (ZMO) frente al norte de Chile y Perú, tratando de entender quienes son los principales involucrados en los ciclos biogeoquímicos de la ZMO y que estrategias metabólicas están utilizando. Para ellos, combinamos técnicas de citometría de flujo, moleculares y aproximaciones biogeoquímicas. La mayor parte de nuestro trabajo, hasta el momento, se ha focalizado en los microbios capaces de realizar fotosíntesis oxigénica, como las cianobacterias, y aquellos involucrados en el ciclo del nitrógeno, como las bacterias desnitrificantes, nitrificantes y anammox. También hemos comenzado a investigar la abundancia y diversidad microbiana en general. En cada caso, estamos encontrando que la ZMO alberga comunidades microbianas propias, ya sea desde una perspectiva filogenética o funcional. En este trabajo presentaremos un resumen de nuestros principales resultados.

Palabras Claves: Zona de mínimo de oxígeno, diversidad microbiana, ciclo del nitrógeno.


INTRODUCTION

In some regions of the global open ocean the low rates of ventilation and the high oxygen demand by the aerobic respiration of the settling organic matter produced in surface waters create a permanent oxygen-deficient layer of a few hundred meters at intermediate depths, the so-called oxygen minimum zone (OMZ). Such is the case in the eastern South Pacific off Peru and northern Chile. The low-oxygen conditions (<20 µM of dissolved O2) in open waters constitute a unique marine pelagic environment, in which microaerophilic, anaerobic and facultative microorganisms flourish, and whose ways of life do not rely on the presence of oxygen, or at least not primarily, as is case for the rest of the ocean. In such an environment, these microorganisms can impact significantly the local, and in some cases the global, biogeochemical cycles. A typical example of OMZ microbial communities of global importance are the denitrifiers, which use nitrate as electron acceptor for the respiration of organic matter reducing it to molecular nitrogen (N2), a gas form that can escape the ocean. However, the recently-discovered anammox process (the anaerobic oxidation of ammonium), which is done by a special group of bacteria (the Planctomycetes) and can also produce N2 as the final product, has been found to occur in OMZs (Kuypers et al. 2005; Thamdrup et al. 2006). These findings are challenging our view of how and by whom elements such as nitrogen are being cycled in these environments.

In the recent years, our group has been studying the microbial communities of the OMZ off Chile trying to understand who the main players are in the biogeochemical cycles and which metabolic strategies they are using. For that we are combining flow cytometry, molecular techniques and biogeochemical approaches. Most of our work so far has focused on the photosynthetic component of the picoplankton and on microbes involved in the nitrogen cycle, but other groups and the general microbial diversity are starting to be investigated. In this presentation we give a summary of our main results.


GENERAL BACTERIOPLANKTON ABUNDANCE AND BACTERIAL DIVERSITY

In most of the global ocean bacterioplankton abundance has a maximum in surface waters, where phytoplankton primary production takes place, and then decreases with depth. In OMZs, however, we have found that there is a secondary maximum at intermediate depths associated with the suboxic waters. This maximum includes both Archaea and Bacteria.

To determine the structure of the bacterial communities associated with the OMZ, the phylogenetic affiliation of sequences derived from two clone libraries from oxygen-deficient waters and two libraries from surface and deeper oxic waters was analyzed based on 16S rRNA gene fragments. The majority of sequences affiliated with bacterial classes commonly found in marine habitats.

However, phylogenetic analysis at the subclass level revealed the presence of a distinct OMZ community, with yet-to-be further characterized specific clusters. Comparison of the bacterial diversity among OMZ, surface and deeper oxic waters, and other marine habitats showed that the OMZ harbors a bacterial community significantly different from surface and underlying oxic waters. Moreover, in contrast to the low macrofaunal diversity found in OMZs, bacterial diversity in the oxygen-deficient waters is found to be higher than in the surrounding waters and comparable with that of general oxygenated marine waters.


PICOCYANOBACTERIA IN OXYGEN-DEFICIENT WATERS

Cyanobacteria of the genus Prochlorococcus and Synechococcus have been found inhabiting the suboxic waters of the upper boundary of the OMZ off northern Chile, where light is still available for photosynthesis. They have been identified and quantified through flow cytometry, high performance liquid chromatography (HPLC), dot blot hybridization and cloning and sequencing of the 16S rRNA genes and the ITS region. These picocyanobacteria have shown to belong to new clades and to fix inorganic carbon efficiently in the suboxic waters at very low light intensities.


BACTERIAL DIVERSITY AND THE NITROGEN CYCLE

Denitrifiers:

Denitrification (the dissimilative reduction of nitrate to N2O and N2) can be done by many groups of microbes distantly related phylogenetically. Therefore, the 16S rRNA approach is not suitable for looking at the diversity of this functional group. We have assessed the structure of the bacterial denitrifying community in the OMZ using the nirS functional marker gene that encodes cd1-containing nitrite reductase, enzyme that catalyzes the reduction of nitrite to nitric oxide, a key step in denitrification. We found shifts in the community structure along biogeochemical gradients, mainly of dissolved oxygen, nitrate and nitrite. Furthermore, we also found, through phylogenetic analysis of environmental sequences, that the nirS genes are from presumably novel and yet uncultivated denitrifiers, which appear to be distantly related to those of the OMZ in the Arabian Sea (Castro-González et al. 2005).

Nitrifiers:

The composition of ammonia-oxidizing bacteria from the b-proteobacteria subclass (bAOB) was studied in the surface and upper oxycline oxic waters and within the OMZ. This study was carried out through cloning and sequencing of genes encoding for the 16S ribosomal RNA and the ammonia monooxygenase enzyme active subunit (amoA). Sequences affiliated to Nitrosospira-like Cluster 1 dominated the 16S rRNA gene clone libraries constructed from both oxic and suboxic waters. Cluster 1 consists exclusively of yet-uncultivated bAOB from marine environments. Sequences in clone libraries of the amoA gene from the surface and upper oxycline could be grouped in a marine subcluster, also containing no cultured representatives. In contrast, all amoA sequences originated from the OMZ were either closely affiliated to cultured Nitrosospira spp. from Cluster 0 or to other yet-uncultured bAOB from soil and aerated_anoxic Orbal process plant, and therefore different from those found in oxic waters. Thus the OMZ has a distinct group of bAOB at the functional level (Molina et al. submitted).

Anammox bacteria:

The existence of the anammox (anaerobic ammonium oxidation) process in the suboxic waters off northern Chile has been recently demonstrated (Thamdrup et al. 2006). We have constructed 16S rRNA clone libraries from the same waters and found the presence of Planctomycetes closely associated with those found in the Black Sea and Benguela upwelling ecosystem (Kuypers et al. 2005). We have also used fluorescence in-situ hybridization (FISH) to quantify the abundance of anammox bacteria and determine their distribution in the water column and found that they are consistent with the anammox rate measurements being measured in the region and elsewhere.


FUTURE WORK

To gain further insight into the diverse genetic and metabolic characteristics of the microorganisms inhabiting the OMZ, particularly in relation to nitrogen and carbon cycling in suboxic waters, the application of environmental genomic techniques is our next step.

ACKNOWLEDGEMENTS

This work has been supported by the Chilean National Commission for Scientific and Technological Research (CONICYT) through the FONDAP, FONDECYT and PBCT Programs, as well as by Fundación Andes, and the Agouron Institute.

REFERENCES

Castro-González, M., G. Braker, L. Farías & O. Ulloa. 2005. Communities of nirS-type denitrifiers in the water column of the oxygen minimum zone in the eastern South Pacific. Environmental Microbiology, 7, 1298-1306.         [ Links ]

Kuypers, M. M. M., G. Lavik, D. Woebken, M. Schmid, B. M. Fuchs, R. Amann, B. B. Jørgensen & M. S. M. Jetten. 2005. Massive nitrogen loss from the Benguela upwelling system through anaerobic ammonium oxidation. Proceedings of the National Academy of Sciences USA, 102, 6478-6483.         [ Links ]

Molina, V., O. Ulloa, L. Farías, H. Urrutia, S. Ramírez, P. Junier & K.-P. Witzel. Ammonia-oxidizing b-proteobacteria from the oxygen minimum zone off northern Chile. Submitted to Applied and Environmental Microbiology.         [ Links ]

Thamdrup, B., T. Dalsgaard, M. M. Jensen, O. Ulloa, L. Farías & R. Escribano. 2006. Anaerobic ammonium oxidation in the oxygen-deficient waters off northern Chile. Limnology and Oceanography, 51, 2145-2156.         [ Links ]

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