Calanus finmarchicus and Calanus glacialis are
keystone zooplankton species in North Atlantic and Arctic
marine ecosystems because they form a link in the trophic
transfer of nutritious lipids from phytoplankton to predators
on higher trophic levels. These calanoid copepods spend several
months of the year in deep waters in a dormant state
called diapause, after which they emerge in surface waters
to feed and reproduce during the spring phytoplankton bloom.
Disruption of diapause timing could have dramatic consequences
for marine ecosystems. In the present study, Calanus
C5 copepodites were collected in a Norwegian fjord during
diapause and were subsequently experimentally exposed to
the water-soluble fraction of a naphthenic North Sea crude
oil during diapause termination. The copepods were sampled
repeatedly while progressing toward adulthood and were analyzed
for utilization of lipid stores and for differential expression
of genes involved in lipid metabolism. Our results
indicate that water-soluble fraction exposure led to a temporary
pause in lipid catabolism, suggested by (i) slower utilization
of lipid stores in water-soluble fraction-exposed C5 copepodites
and (ii) more genes in the b-oxidation pathway being
downregulated in water-soluble fraction-exposed C5 copepodites
than in the control C5 copepodites. Because lipid content
and/or composition may be an important trigger for termination
of diapause, our results imply that the timing of
diapause termination and subsequent migration to the surface
may be delayed if copepods are exposed to oil pollution during
diapause or diapause termination. This delay could have
detrimental effects on ecosystem dynamics.
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The beta-oxidation pathway is downregulated during diapause termination in Calanus copepods
Calanus copepods are keystone species in marine ecosystems, mainly due to their high lipid content,
which is a nutritious food source for e.g. juvenile fish. Accumulated lipids are catabolized to meet
energy requirements during dormancy (diapause), which occurs during the last copepodite stage (C5).
The current knowledge of lipid degradation pathways during diapause termination is limited. We
characterized changes in lipid fullness and generated transcriptional profiles in C5s during termination
of diapause and progression towards adulthood. Lipid fullness of C5s declined linearly during
developmental progression, but more β-oxidation genes were upregulated in early C5s compared to
late C5s and adults. We identified four possible master regulators of energy metabolism, which all
were generally upregulated in early C5s, compared to late C5s and adults. We discovered that one
of two enzymes in the carnitine shuttle is absent from the calanoid copepod lineage. Based on the
geographical location of the sampling site, the field-samples were initially presumed to consist of
C. finmarchicus. However, the identification of C. glacialis in some samples underlines the need for
performing molecular analyses to reliably identify Calanus species. Our findings contributes to a better
understanding of molecular events occurring during diapause and diapause termination in calanoid
copepods.
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- Award ID(s):
- 1746087
- NSF-PAR ID:
- 10171451
- Date Published:
- Journal Name:
- Scientific reports
- Volume:
- 9
- ISSN:
- 0068-1261
- Page Range / eLocation ID:
- 16686
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Late developmental stages of the marine copepods in the genus
Calanus can spend extended periods in a dormant stage (diapause) that is preceded by the accumulation of large lipid stores. We assessed how lipid metabolism during development from the C4 stage to adult is altered in response to predation risk and varying food availability, to ultimately understand more of the metabolic processes during development inCalanus copepods. We used RNA sequencing to assess if perceived predation risk in combination with varied food availability affects expression of genes associated with lipid metabolism and diapause preparation inC. finmarchicus . The lipid metabolism response to predation risk differed depending on food availability, time and life stage. Predation risk caused upregulation of lipid catabolism with high food, and downregulation with low food. Under low food conditions, predation risk disrupted lipid accumulation. The copepods showed no clear signs of diapause preparation, supporting earlier observations of the importance of multiple environmental cues in inducing diapause inC. finmarchicus . This study demonstrates that lipid metabolism is a sensitive endpoint for the interacting environmental effects of predation pressure and food availability. As diapause may be controlled by lipid accumulation, our findings may contribute towards understanding processes that can ultimately influence diapause timing. -
In high-latitude environments where seasonal changes include periods of harsh conditions, many arthropods enter diapause, a period of dormancy that is hormonally regulated. Diapause is characterized by very low metabolism, resistance to environmental stress, and developmental arrest. It allows an organism to optimize the timing of reproduction by synchronizing offspring growth and development with periods of high food availability. In species that enter dormancy as pre-adults or adults, termination of diapause is marked by the resumption of physiological processes, an increase in metabolic rates and once transitioned into adulthood for females, the initiation of oogenesis. In many cases, individuals start feeding again and newly acquired resources become available to fuel egg production. However, in the subarctic capital-breeding copepod Neocalanus flemingeri, feeding is decoupled from oogenesis. Thus, optimizing reproduction limited by fixed resources such that all eggs are of high quality and fully-provisioned, requires regulation of the number of oocytes. However, it is unknown if and how this copepod limits oocyte formation. In this study, the phase in oocyte production by post-diapause females that involved DNA replication in the ovary and oviducts was examined using incubation in 5-Ethynyl-2′-deoxyuridine (EdU). Both oogonia and oocytes incorporated EdU, with the number of EdU-labeled cells peaking at 72 hours following diapause termination. Cell labeling with EdU remained high for two weeks, decreasing thereafter with no labeling detected by four weeks post diapause, and three to four weeks before spawning of the first clutch of eggs. The results suggest that oogenesis is sequential in N. flemingeri with formation of new oocytes starting within 24 hours of diapause termination and limited to the first few weeks. Lipid consumption during diapause was minimal and relatively modest initially. This early phase in the reproductive program precedes mid-oogenesis and vitellogenesis 2, when oocytes increase in size and accumulate yolk and lipid reserves. By limiting DNA replication to the initial phase, the females effectively separate oocyte production from oocyte provisioning. A sequential oogenesis is unlike the income-breeder strategy of most copepods in which oocytes at all stages of maturation are found concurrently in the reproductive structures.more » « less
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Synopsis In high-latitude environments where seasonal changes include periods of harsh conditions, many arthropods enter diapause, a period of dormancy that is hormonally regulated. Diapause is characterized by very low metabolism, resistance to environmental stress, and developmental arrest. It allows an organism to optimize the timing of reproduction by synchronizing offspring growth and development with periods of high food availability. In species that enter dormancy as pre-adults or adults, termination of diapause is marked by the resumption of physiological processes, an increase in metabolic rates and once transitioned into adulthood for females, the initiation of oogenesis. In many cases, individuals start feeding again and newly acquired resources become available to fuel egg production. However, in the subarctic capital-breeding copepod Neocalanus flemingeri, feeding is decoupled from oogenesis. Thus, optimizing reproduction limited by fixed resources such that all eggs are of high quality and fully-provisioned, requires regulation of the number of oocytes. However, it is unknown if and how this copepod limits oocyte formation. In this study, the phase in oocyte production by post-diapause females that involved DNA replication in the ovary and oviducts was examined using incubation in 5-Ethynyl-2′-deoxyuridine (EdU). Both oogonia and oocytes incorporated EdU, with the number of EdU-labeled cells peaking at 72 hours following diapause termination. Cell labeling with EdU remained high for two weeks, decreasing thereafter with no labeling detected by four weeks post diapause, and three to four weeks before spawning of the first clutch of eggs. The results suggest that oogenesis is sequential in N. flemingeri with formation of new oocytes starting within 24 hours of diapause termination and limited to the first few weeks. Lipid consumption during diapause was minimal and relatively modest initially. This early phase in the reproductive program precedes mid-oogenesis and vitellogenesis 2, when oocytes increase in size and accumulate yolk and lipid reserves. By limiting DNA replication to the initial phase, the females effectively separate oocyte production from oocyte provisioning. A sequential oogenesis is unlike the income-breeder strategy of most copepods in which oocytes at all stages of maturation are found concurrently in the reproductive structures.
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Abstract The high-latitude copepod Neocalanus flemingeri exploits the spring phytoplankton bloom to accumulate lipids for survival during food-limited periods and to fuel reproduction. At some point during development, lipid-accumulation ends and pre-adults molt into adults, descend to depth and enter a state of dormancy termed diapause. How and when they determine to make this transition is still unresolved. According to one hypothesis, the trigger is their attaining a threshold amount of lipid fullness. Alternatively, they might follow a genetic program, entering diapause within a narrow developmental window. To better understand the decision, a 5-week laboratory experiment was conducted to assess the effect of food quantity and type on lipid accumulation, biomass and gene expression in N. flemingeri copepodite stage CV. In fed individuals, the initial rate of lipid accumulation slowed by week 5, as a portion of CVs began to molt into adults. While changes in gene expression common to all fed individuals between weeks 1 and 3 were consistent with a developmental program, the duration of the CV stage was variable. Unfed individuals maintained lipid stores initially, suggesting physiological acclimatization to conserve energy. A comparison with gene expression profiles of field-collected individuals suggests similar responses to resources in the environment.
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/https://doi.org/10.1038/s41598-019-53032-5
