The first report of a microdiverse anammox bacteria
community in waters of Colombian Pacific, a transition
area between prominent oxygen minimum zones of the
eastern tropical Pacific
M. Castro-González,
1
* V. Molina,
2
E. Rodríguez-Rubio
3,4
and O. Ulloa
5
1
Laboratorio de Ecología Microbiana, Universidad del
Tolima, Ibagué, Colombia.
2
Departamento de Biología, Facultad de Ciencias
Naturales y Exactas, Universidad de Playa Ancha,
Valparaíso, Chile.
3
Centro de Investigaciones Oceanográficas e
Hidrográficas del Pacífico, Tumaco, Colombia.
4
Asesor, Instituto Colombiano del Petróleo,
Piedecuesta, Colombia.
5
Departamento de Oceanografía, e Instituto Milenio de
Oceanografía, Universidad de Concepción, Concepción,
Chile.
Summary
Anaerobic ammonium oxidizers contribute to the
removal of fixed nitrogen in oxygen-deficient marine
ecosystems such as oxygen minimum zones (OMZ).
Here we surveyed for the first time the occurrence
and diversity of anammox bacteria in the Colombian
Pacific, a transition area between the prominent
South and North Pacific OMZs. Anammox bacteria
were detected in the coastal and oceanic areas of the
Colombian Pacific in low oxygen (< 22 μM), high
nitrate (25–35 μM) and low nitrite (< 0.07 μM),
and ammonium (< 1 μM) waters. In these waters,
anammox bacteria were rich [∼ 7 operational taxo-
nomic units (OTUs), 98% cut-off) and microdiverse
(Shannon index H′< 1.24), in comparison with the
observed at the prominent OMZ of the Eastern
Tropical South Pacific, Arabian Sea and Black Sea.
Anammox bacteria-like sequences from the Colom-
bian Pacific were grouped together with sequences
retrieved from the distinct OMZ’s marine subclu-
sters (Peru, Northern Chile and Arabian Sea)
within Candidatus ‘Scalindua spp’. Moreover, some
anammox bacteria OTUs shared a low similarity with
environmental phylotypes (86–94%). Our results indi-
cated that a microdiverse anammox community
inhabits the Colombian Pacific, generating new ques-
tions about the ecological and biogeochemical differ-
ences influencing its community structure.
Introduction
Anaerobic ammonium oxidation (Anammox) consists of a
short circuit in the nitrogen gaseous formation of nitrogen
cycling, providing an alternative pathway to the coupled
nitrification–denitrification process (Mulder et al., 1995).
The anammox process contributes to approximately
30–60% of the nitrogen loss in the ocean and has been
estimated to account for between one-fifth and essentially
all of the N
2 production in marine oxygen minimum zones
(OMZ) (Dalsgaard et al., 2005; Kuypers et al., 2005). One
of the most extensive surveys of anammox versus
denitrification measurements recently carried out in the
eastern south Pacific Ocean (ESPO) identified that
anammox activity with maximum rates of 0.85 nmol
N
2 L
−1
h
−1
was mainly centred in shallow anoxic depths
(Dalsgaard et al., 2012). This was consistent with previous
studies developed in the area (Hamersley et al., 2007;
Galán et al., 2009; Lam et al., 2009; Ward et al., 2009).
Anammox bacteria are phylogenetically constrained
within a monophyletic deep branch in the order
Planctomycetales, consisting of three Candidatus genera:
Brocadia, Kuenenia and Scalindua. Scalindua-like
anammox bacteria are the most commonly detected in
many worldwide aquatic habitats such as OMZ and
anoxic or suboxic marine waters (Dalsgaard et al.,
2003; Kuypers et al., 2003; 2005; Hamersley et al.,
2007; Lam et al., 2007; Woebken et al., 2008; Galán
et al., 2009; 2012), marine and estuarine sediments
(Dalsgaard and Thamdrup, 2002; Trimmer et al., 2003;
Risgaard-Petersen et al., 2004; Rysgaard et al., 2004;
Rich et al., 2008; Dale et al., 2009; Dang et al., 2010;
Hirsh et al., 2011), and freshwater ecosystems (Penton
et al., 2006; Schubert et al., 2006; Zhang et al., 2007;
Hamersley et al., 2009; Wenk et al., 2013). However,
anammox survey studies using 16S rRNA, ITS and the
Received 8 July, 2013; accepted 1 April, 2014. *For correspondence.
E-mail mcastro@ut.edu.co; Tel. 57(8)2772049; Fax 57(8)2772049.
Environmental Microbiology Reports (2014) doi:10.1111/1758-2229.12165
© 2014 Society for Applied Microbiology and John Wiley & Sons Ltd