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Variations in Copepod Proteome and Respiration Rate in Association with Diel Vertical Migration and Circadian Cycle

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Variations in Copepod Proteome and Respiration Rate in Association with Diel Vertical Migration and Circadian Cycle Reference: Biol. Bull. 235: 30–42. (August 2018) © 2018 The University of Chicago Variations in Copepod Proteome and Respiration Rate in Association with Diel Vertical Migration and Circadian Cycle 1,* 1 2 3 AMY E. MAAS , LEOCADIO BLANCO-BERCIAL , ALI LO , ANN M. TARRANT , 2 AND EMMA TIMMINS-SCHIFFMAN 1Bermuda Institute of Ocean Sciences, 17 Biological Station, St. George’s GE01, Bermuda; 2Department of Genome Sciences, University of Washington, Seattle, Washington 98195; and 3Biology Department, Woods Hole Oceanographic Institution, 266 Woods Hole Road, Woods Hole, Massachusetts 02543 Abstract. The diel vertical migration of zooplankton is a respiration experiments, which show an underlying cycle in process during which individuals spend the night in surface metabolic rate, with a peak at dawn. This project generates mo- waters and retreat to depth during the daytime, with substan- lecular tools (transcriptome and proteome) that will allow for tial implications for carbon transport and the ecology of mid- more detailed understanding of the underlying physiological water ecosystems. The physiological consequences of this daily processes that influence and are influenced by diel vertical mi- pattern have, however, been poorly studied beyond investiga- gration. Further, these studies suggest that P. xiphias is a trac- tions of speed and the energetic cost of swimming. Many other table model for continuing investigations of circadian and diel processes are likely influenced, such as fuel use, energetic trade- vertical migration influences on plankton physiology. Previous offs, underlying diel (circadian) rhythms, and antioxidant re- studies did not account for this cyclic pattern of respiration and sponses. Using a new reference transcriptome, proteomic may therefore have unrepresented respiratory carbon fluxes analyses were applied to compare the physiological state of from copepods by about 24%. a migratory copepod, Pleuromamma xiphias, immediately after arriving to the surface at night and six hours later. Ox- ygen consumption was monitored semi-continuously to ex- Introduction plore underlying cyclical patterns in metabolic rate under dark- One of the greatest cyclical patterns in the pelagic ecosystem dark conditions. The proteomic analysis suggests a distinct shift is the daily migration of various zooplankton and fish to depth, in physiology that reflects migratory exertion and changes in a process referred to as diel vertical migration (DVM). DVM is metabolism. These proteomic analyses are supported by the typified by the presence of transient species in the warm, oxy- genated, photic zone during the night, followed by a movement Received 22 January 2018; Accepted 11 June 2018; Published online of individuals into colder, deeper water during the day (al- August 16, 2018. though variations, including reverse migrations, exist; Hey- * To whom correspondence should be addressed. E-mail: amy.maas@bios wood, 1996; Hays, 2003). These daily migrations are thought .edu. to be energetically expensive, with individuals smaller than Abbreviations: ACN, acetonitrile; ANOSIM, analysis of similarity; 1 cm traveling hundreds of meters per day. DVM speed has BATS, Bermuda Atlantic Time Series; BUSCO, Benchmarking Universal Single-Copy Orthologs; DM, dry mass; DVM, diel vertical migration; been estimated, via calculations of the observed amplitude FFT-NLLS, fast Fourier transform non-linear least squares; GO, gene ontol- and duration of DVM for copepods and euphausiids, to range 21 ogy; MESA, maximum entropy spectral analysis; NAD, nicotinamide ade- between 10 and 55 mm s (Wiebe et al., 1992; Mauchline, nine dinucleotide; NAD1, oxidized nicotinamide adenine dinucleotide; 1998). The estimates of the physiological costs of such pro- NADH, reduced nicotinamide adenine dinucleotide; NMDS, non-metric found exertion, based on force transducer and video analyses, multidimensional scaling; nr, non-redundant database; NSAF, normalized spectral abundance factor; RT, room temperature; TTP, Trans Proteomic range between 13% and 120% of copepod basal metabolic rate Pipeline. (reviewed in Mauchline, 1998). Despite the costs, the process Online enhancements: data files. is believed to provide a number of advantages to migratory or- 30 This content downloaded from 128.111.205.145 on October 06, 2018 13:08:10 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). DIEL CHANGES IN COPEPOD PHYSIOLOGY 31 ganisms, including niche partitioning, metabolic advantage circadian clock (Enright and Hamner, 1967), thus suggesting due to colder temperatures at depth, retreat from light or high that there is still much to be learned in this system. temperatures, and, most importantly, predator avoidance (Hays, New advances in molecular techniques have recently opened 2003; Antezana, 2009). the door for more detailed analyses of these more complex as- Globally, the DVM of the zooplankton community is esti- pects of DVM, and research regarding the influence of circa- mated to be responsible for 15%–40% of the total organic dian patterns on diel and seasonal migrations is underway carbon export from the surface to the mesopelagic (Steinberg (Cohen and Forward, 2009; Teschke et al., 2011; Christie et al., 2000; Bianchi and Mislan, 2016), exceeding in many et al., 2013; De Pitta et al., 2013). A recent analysis using cases the carbon flux related to passively sinking particles semi-continuous optical oxygen sensing, characterization of (Kobari et al., 2003, 2008; Steinberg et al., 2008; Steinberg DVM behavior, and expression of core clock genes via quan- and Landry, 2017). Similar percentages are reported for the titative polymerase chain reaction (qPCR) revealed that the nitrogen-related processes (e.g., Dam et al., 1995; Al-Mutairi copepod Calanus finmarchicus has a true circadian rhythm and Landry, 2001; Schnetzer and Steinberg, 2002b; Stein- in metabolism, with a suggested peak in respiration during berg et al., 2002). These estimates are typically made by apply- the early evening (Häfker et al., 2017). This sets the stage ing mass-specific and temperature-scaling factors to experi- for studies that investigate which other processes may also be mentally calculated oxygen consumption, as well as nitrogen influenced by both migratory behavior and circadian cycles. and carbon excretion by individual organisms. These experi- The goal of this project was to determine whether it is pos- ments are traditionally done by placing individuals in bottles sible to observe biogeochemically relevant diel changes in the for long durations (8–24 h), with no mention of the start time physiology of a subtropical copepod through organismal (res- of the experiment; and, thus, variations in physiological state piration) and molecular (proteomics) methods. To support the that are a consequence of circadian patterns or the DVM pro- latter analysis, we generated a species-specific copepod tran- cess are lost. If there are substantial physiological changes scriptome that could then be used to identify copepod proteins associated with migration or hidden daily cycles in major phys- and to detail the change in protein abundances that a vertical iological processes, such as oxygen consumption and ammo- migratory zooplankton experiences over the nighttime por- nia excretion, they may cause errors in the estimations of tion of its diel cycle. Pleuromamma xiphias, a well-known organismal contributions to biogeochemical flux during day- vertical migrator at the Bermuda Atlantic Time Series (BATS) time at depth. Previous studies have suggested that this may in- site, was chosen for this study because it has previously been deed be the case, with the migratory copepods Pleuromamma shown to have diel patterns in respiration rate that are assumed xiphias and Calanus euxinus showing substantially higher res- to be associated with its migratory behavior (Pavlova, 1994). piration rates late in the evening (22:00) and early in the morn- This species is abundant in the Sargasso Sea, and its contribu- ing (05:00) relative to the nadir at mid-day (13:00) (Pavlova, tions to nitrogen and carbon flux have previously been charac- 1994). The design of these studies still relied upon noncon- terized using classical bottle sampling methods (Wormuth, tinuous respirometry measurements (3–6-h endpoint incuba- 1981; Steinberg et al., 2000, 2002; Schnetzer and Steinberg, tions), making a pinpointed analysis of the variation in physi- 2002b; Teuber et al., 2013), providing greater context for the ological response impossible. more detailed physiological assessment enabled by proteomics To explore the physiological signature of DVM, more analysis. finely resolved measurements are required. Furthermore, al- though it is important to define the energetic cost of swim- ming, understanding the full physiological implications of Materials and Methods migrations requires analysis of more complex mechanisms Copepod collection for transcriptomic such as changes in metabolic pathways, endogenous circa- and proteomic analyses dian rhythms, and antioxidant activity. These topics have been explored in terrestrial migratory studies (i.e., Gwinner and Female copepods (Pleuromamma xiphias (Giesbrecht, 1889)) Helm, 2003; McGuire and Guglielmo, 2009; Skrip and Mc- were collected off the coast of Bermuda (31739.93N, Williams, 2016) but have not, to date, received much attention 64700.14W; 31732.00N, 63737.02W) near the BATS site. in zooplankton because of the difficulty of organismal sam- Sampling
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