1 3
Mar Biol (2014) 161:575–584
DOI 10.1007/s00227-013-2360-z
ORIGINAL PAPER
Hypoxia-driven selective degradation of cellular proteins
in jumbo squids during diel migration to the oxygen minimum
zones
Katja Trübenbach · Gonçalo da Costa ·
Cristina Ribeiro-Silva · Raquel Mesquita Ribeiro ·
Carlos Cordeiro · Rui Rosa
Received: 25 April 2013 / Accepted: 20 November 2013 / Published online: 11 December 2013
© Springer-Verlag Berlin Heidelberg 2013
role in hypoxia tolerance, but further investigations are nec-
essary to discover its full potential and pathways.
Introduction
The jumbo or Humboldt squid (Dosidicus gigas) is a jet-
propelled oceanic top predator endemic to the Eastern
Pacific, and one of its most pronounced features is the abil-
ity to perform diel vertical migrations into oxygen mini-
mum zones (OMZs). Consequently, it spends >70 % of
the daytime below its critical oxygen partial pressure (P
crit
,
~1.6 kPa; Gilly et al. 2006; Seibel 2013). It is worth not-
ing that active muscular squids were thought to be pre-
cluded from hypoxic areas (Pörtner 2002), as consequence
of their physiological and anatomical restraints (Pörtner
1994, 2002; Melzner et al. 2007). Unexpectedly, D. gigas
thrives in mesopelagic OMZs via metabolic suppression
(Rosa and Seibel 2008, 2010; Trübenbach et al. 2013).
Marine organisms exposed to hypoxia commonly suppress
their metabolism by 50–95 %, as energy reserve stores are
limited and fermentative pathways less efficient, and sup-
plement the remaining energy demand using a combination
of aerobic (oxidative phosphorylation) and anaerobic meta-
bolic pathways (Seibel 2011). The main biochemical fuel
under hypoxia is glycogen (i.e., gastropods, bivalves, and
sluggish fish; Shulman et al. 2002), but in squids, glyco-
gen reserves are less than 0.4 % of body weight (Rosa et al.
2005a, b), and therefore, a few minutes of activity can sig-
nificantly deplete them (Storey and Storey 1983). Moreo-
ver, cephalopods, under well-oxygenated conditions, feed
on proteins (O’Dor and Webber 1986; Lamarre et al. 2012),
and available evidence does indicate that squids, at least,
under extreme conditions like at the end of their migrations
show high levels of muscle proteolysis due to fasting and
Abstract The jumbo squid, Dosidicus gigas, is an oce-
anic top predator in the eastern tropical Pacific that under-
goes diel vertical migrations into mesopelagic oxygen
minimum zones (OMZs). Besides glycogen breakdown,
the pathways of the squid’s metabolic (suppression) strat-
egy are poorly understood. Here, juvenile D. gigas were
exposed to oxygen levels found in the OMZ off Gulf of
California (1 % O
2
, 1 kPa at 10 °C) with the aim to identify,
via proteomic tools, eventual anaerobic protein degradation
as potential energy source at such depths. Under hypoxia,
total protein concentration decreased nonsignificantly
from 79.2 ± 12.4 mg g
-1
wet mass to 74.7 ± 11.7 mg g
-1
wet mass (p > 0.05). Yet, there was a significant decrease
in heat-shock protein (Hsp) 90 and α-actinin contents
(p < 0.05). The lower α-actinin concentration at late
hypoxia was probably related to decreased protection of the
Hsp90 chaperon machinery resulting in increased ubiqui-
tination (p < 0.05) and subsequent degradation. Thus, the
present findings indicate that D. gigas might degrade, at
least under progressing hypoxia, specific mantle proteins
anaerobically to increase/maintain anaerobic ATP pro-
duction and extend hypoxia exposure time. Moreover, the
ubiquitin–proteasome system seems to play an important
Communicated by H.-O. Pörtner.
K. Trübenbach (*) · R. Rosa
Laboratório Marítimo da Guia, Centre of Oceanography,
University of Science in Lisbon, Av. Nossa Senhora do Cabo 939,
2750-374 Cascais, Portugal
e-mail: kjtrubenbach@fc.ul.pt
G. da Costa · C. Ribeiro-Silva · R. M. Ribeiro · C. Cordeiro
Department of Chemistry and Biochemistry,
University of Science in Lisbon, Campo Grande,
1749-016 Lisbon, Portugal