Maintenance of Complex Life Cycles Via Cryptic Differences In The Ecophysiology Of Haploid And Diploid Spores Of An Isomorphic Red Alga1.

Recognition of the wide diversity of organisms that maintain complex haploid-diploid life cycles has generated interest in understanding the evolution and persistence of such life cycles. We empirically tested the model where complex haploid-diploid life cycles may be maintained by subtle/cryptic differences in the vital rates of isomorphic haploid-diploids, by examining the ecophysiology of haploid tetraspores and diploid carpospores of the isomorphic red alga Chondrus verrucosus. While tetraspores and carpospores of this species did not differ in size or autofluorescence, concentrations of phycobiliproteins of carpospores were greater than that of tetraspores. However, tetraspores were more photosynthetically competent than carpospores over a broader range of photosynthetic photon flux densities (PPFDs) and at PPFDs found at both the depth that C. verrucosus is found at high tide and in surface waters in which planktonic propagules might disperse. These results suggest potential differences in dispersal potential and reproductive success of haploid and diploid spores. Moreover, these cryptic differences in ecological niche partitioning of haploid and diploid spores contribute to our understanding of some of the differences between these ploidy stages that may ultimately lead to the maintenance of the complex haploid-diploid life cycle in this isomorphic red alga.

Sneaker Male Squid Produce Long-lived Spermatozoa by Modulating Their Energy Metabolism.

Spermatozoa released by males should remain viable until fertilization. Hence, sperm longevity is governed by intrinsic and environmental factors in accordance with the male mating strategy. However, whether intraspecific variation of insemination modes can impact sperm longevity remains to be elucidated. In the squid Heterololigo bleekeri, male dimorphism (consort and sneaker) is linked to two discontinuous insemination modes that differ in place and time. Notably, only sneaker male spermatozoa inseminated long before egg spawning can be stored in the seminal receptacle. We found that sneaker spermatozoa exhibited greater persistence in fertilization competence and flagellar motility than consort ones because of a larger amount of flagellar glycogen. Sneaker spermatozoa also showed higher capacities in glucose uptake and lactate efflux. Lactic acidosis was considered to stabilize CO2-triggered self-clustering of sneaker spermatozoa, thus establishing hypoxia-induced metabolic changes and sperm survival. These results, together with comparative omics analyses, suggest that postcopulatory reproductive contexts define sperm longevity by modulating the inherent energy levels and metabolic pathways.

Arrest at metaphase of meiosis I in starfish oocytes in the ovary is maintained by high CO2 and low O2 concentrations in extracellular fluid.

During the spawning process in starfish, oocytes are arrested at metaphase of meiosis I (MI) within the ovary, and reinitiate meiosis only after they have been released into the seawater. However, this arrest does not occur if the ovary is removed from the animal. As the pH of the coelomic fluid is buffered by CO2/H(+)/HCO3(-), we investigated the involvement of gas concentrations in MI arrest. In vivo, the CO2 level in the coelomic fluid was high (∼1.5% vs. 0.04% in air) and the O2 level was low (0.1-1.0% vs. ∼20% in air). When these gas conditions were reproduced in isolated coelomic fluid or seawater, ovarian oocytes arrested at MI, just as in vivo. Isolated oocytes from the ovary required the similar high CO2 and low O2 level to remain arrested in MI and had an intracellular pH of ∼6.9. Intracellular pH increased to ∼7.3 when oocytes were transferred to seawater equilibrated with air, a condition that mimics that of spawning. We used ammonium acetate to clamp intracellular pH at different levels and found that MI arrest occurred when intracellular pH was ∼6.9. Our results support the idea that high CO2 and low O2 in the ovarian environment lead to low intracellular pH and MI arrest, while spawning into the seawater with low CO2 and high O2 results in high intracellular pH and release from MI arrest. The biological significance of MI arrest is that oocytes are spawned into seawater at the optimal physiological state of MI when the least polyspermy occurs.

Reproduction in cultured versus wild coral colonies: fertilization, larval oxygen consumption, and survival.

In the late 1990s, the once prolific populations of the coral Acropora intermedia surrounding Okinawa, Japan, dramatically declined because of thermal stress, bleaching caused by heat stress, and consequent mortality. Before the bleaching event, 72 fragments (about 15 cm in length) were collected and transferred to the Okinawa Churami Aquarium. Through growth and repeated fragmentation, these original fragments developed into about 100 colonies that spawned from 1999 to 2009. In this study, we compared gametogenesis, fertilization, survival, and O(2) consumption in cultured and wild colonies of A. intermedia and their offspring. Cultured A. intermedia had larger oocytes and higher fertilization and survival rates than samples from wild colonies. O(2) consumption of cultured embryos was similar to that of wild embryos. These results suggest that cultured A. intermedia and their offspring are as viable as wild colonies. Aquaria can play a role in the conservation of endangered corals, and their cultured colonies could be used to re-establish devastated species on the Okinawa reefs.

Substantial energy expenditure for locomotion in ciliates verified by means of simultaneous measurement of oxygen consumption rate and swimming speed.

In order to characterize the energy expenditure of Paramecium, we simultaneously measured the oxygen consumption rate, using an optic fluorescence oxygen sensor, and the swimming speed, which was evaluated by the optical slice method. The standard metabolic rate (SMR, the rate of energy consumption exclusively for physiological activities other than locomotion) was estimated to be 1.18x10(-6) J h(-1) cell(-1) by extrapolating the oxygen consumption rate into one at zero swimming speed. It was about 30% of the total energy consumed by the cell swimming at a mean speed of 1 mm s(-1), indicating that a large amount of the metabolic energy (about 70% of the total) is consumed for propulsive activity only. The mechanical power liberated to the environment by swimming Paramecium was calculated on the basis of Stokes' law. This power, termed Stokes power, was 2.2x10(-9) J h(-1) cell(-1), indicating extremely low efficiency (0.078%) in the conversion of metabolic power to propulsion. Analysis of the cost of transport (COT, the energy expenditure for translocation per units of mass and distance) revealed that the efficiency of energy expenditure in swimming increases with speed rather than having an optimum value within a wide range of forced swimming, as is generally found in fish swimming. These characteristics of energy expenditure would be unique to microorganisms, including Paramecium, living in a viscous environment where large dissipation of the kinetic energy is inevitable due to the interaction with the surrounding water.

Low oxygen consumption and high body content of catch connective tissue contribute to low metabolic rate of sea cucumbers.

The energy consumption of echinoderms is low in comparison with that of other invertebrates. We demonstrated this by measuring the oxygen consumption rate per unit of body weight (VO2) of the sea cucumber Actinopyga mauritiana: VO2 was 1/8 that of the "standard" invertebrates. Low energy consumption in echinoderms has been attributed to their high skeletal content and to catch connective tissues (CCTs) that maintain body posture by altering their mechanical properties with little energy expenditure. The former is not applicable to holothurians, and the latter has not been proven experimentally. We postulated that the large content of dermal connective tissue, which maintaines posture economically, contributes to the low energy consumption in holothurians. Body-wall dermis occupied 53.5% of wet body weight, whereas body-wall muscles, including those of tube feet, occupied 5.1%. VO2 of the dermis in the stiff state (2.45 microl x g(-1) x h(-1)) was 1/10 that of the longitudinal body-wall muscle in contraction. the mechanical tests revealed that the stress at an imposed strain of 2% strain was 7 times greater in CCT than in muscles. These results showed that CCT could maintain posture more economically than muscles could. We concluded that the high content of connective tissue with energy-saving posture-maintenance activities contributed to the low energy consumption of holothurians.

Experimental allometry: effect of size manipulation on metabolic rate of colonial ascidians.

The allometric scaling of metabolic rate of organisms, the three-quarters power rule, has led to a questioning of the basis for the relation. We attacked this problem experimentally for the first time by employing the modular organism, the ascidian that forms a single layered flat colony, as a model system. The metabolic rate and colony size followed the three-quarters power relation, which held even after the colony size was experimentally manipulated. Our results established that the three-quarters power relation is a real continuous function, not an imaginary statistical regression. The fact that all the hypotheses failed to explain why the two-dimensional organism adhered to the three-quarters power relation led us to propose a new hypothesis, in which the allometric relation derives from the self-organized criticality based on local interaction between modulus-comprising organisms.

Switching of metabolic-rate scaling between allometry and isometry in colonial ascidians.

The metabolic rate and its scaling relationship to colony size were studied in the colonial ascidian Botrylloides simodensis. The colonial metabolic rate, measured by the oxygen consumption rate (V(O2) in millilitres of O(2) per hour) and the colony mass (wet weight M(w) in grams) showed the allometric relationship (V(O2) = 0.0412 M(w)(0.799). The power coefficient was statistically not different from 0.75, the value for unitary organisms. The size of the zooids and the tunic volume fraction in a colony were kept constant irrespective of the colonial size. These results, together with the two-dimensional colonial shape, excluded shape factors and colonial composition as possible causes of allometry. Botryllid ascidians show a takeover state in which all the zooids of the parent generation in a colony degenerate and zooids of a new generation develop in unison. The media for connection between zooids such as a common drainage system and connecting vessels to the common vascular system experienced reconstruction. The metabolic rate during the takeover state was halved and was directly proportional to the colonial mass. The scaling thus changed from being allometric to isometric. The alteration in the scaling that was associated with the loss of the connection between the zooids strongly support the hypothesis that the allometry was derived from mutual interaction among the zooids. The applicability of this hypothesis to unitary organisms is discussed.