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1.
Michal Sorek Yosef Z. Yacobi Modi Roopin Ilana Berman-Frank Oren Levy 《Proceedings. Biological sciences / The Royal Society》2013,280(1759)
Biological clocks are self-sustained endogenous timers that enable organisms (from cyanobacteria to humans) to anticipate daily environmental rhythms, and adjust their physiology and behaviour accordingly. Symbiotic corals play a central role in the creation of biologically rich ecosystems based on mutualistic symbioses between the invertebrate coral and dinoflagellate protists from the genus Symbiodinium. In this study, we experimentally establish that Symbiodinium photosynthesis, both as a free-living unicellular algae and as part of the symbiotic association with the coral Stylophora pistillata, is ‘wired’ to the circadian clock mechanism with a ‘free-run’ cycle close to 24 h. Associated photosynthetic pigments also showed rhythmicity under light/dark conditions and under constant light conditions, while the expression of the oxygen-evolving enhancer 1 gene (within photosystem II) coincided with photosynthetically evolved oxygen in Symbiodinium cultures. Thus, circadian regulation of the Symbiodinium photosynthesis is, however, complicated as being linked to the coral/host that have probably profound physiochemical influence on the intracellular environment. The temporal patterns of photosynthesis demonstrated here highlight the physiological complexity and interdependence of the algae circadian clock associated in this symbiosis and the plasticity of algae regulatory mechanisms downstream of the circadian clock. 相似文献
2.
Maribel García Ramos Anastazia T. Banaszak 《Marine biotechnology (New York, N.Y.)》2014,16(2):193-201
The importance of the dinoflagellate Symbiodinium sp. was studied in the early life stages of the gastropod Strombus gigas. This dinoflagellate was not found in the eggs or the gelatinous mass surrounding the eggs of the mollusk; therefore, Symbiodinium is not inherited directly. To determine whether the planktonic veligers can acquire these algae from the environment, they were exposed to freshly isolated Symbiodinium from adult S. gigas (homologous). The optimal stage for Symbiodinium inoculation was found at 48 h post-hatching. Survival and growth rates of veligers and juveniles were higher when inoculated with freshly isolated Symbiodinium in conjunction with daily feeding of Isochrysis spp. Veligers inoculated with Symbiodinium freshly isolated from three host species elicited distinct responses: (1) veligers did not take up Symbiodinium isolated from the hydrozoan Millepora alcicornis suggesting that there is discrimination on contact prior to ingestion, (2) veligers did take up Symbiodinium isolated from the anemone Bartholomea annulata, but the algae did not persist in the host tissue suggesting that selection against this type took place after ingestion or that the algae did not divide in the host, and (3) veligers did take up Symbiodinium isolated from Pterogorgia anceps where it persisted and was associated with metamorphosis of the larvae. In contrast, the Symbiodinium freshly isolated from S. gigas were not associated with metamorphosis and required an inducer such as the red alga Laurencia poitei. These data present a significant advancement for the establishment of a new approach in the aquaculture of this important but declining Caribbean species. 相似文献
3.
Symbiotic corals, which are benthic organisms intimately linked with their environment, have evolved many ways to deal with fluctuations in the local marine environment. One possible coping mechanism is the endogenous circadian clock, which is characterized as free running, maintaining a ~24 h periodicity of circuits under constant stimuli or in the absence of external cues. The quantity and quality of light were found to be the most influential factors governing the endogenous clock for plants and algae. Unicellular dinoflagellate algae are among the best examples of organisms that exhibit circadian clocks using light as the dominant signal. This study is the first to examine the effects of light intensity and quality on the rhythmicity of photosynthesis in the symbiotic dinoflagellate Symbiodinium sp., both as a free-living organism and in symbiosis with the coral Stylophora pistillata. Oxygen production measurements in Symbiodinium cultures exhibited rhythmicity with a periodicity of approximately 24 h under constant high light (LL), whereas under medium and low light, the cycle time increased. Exposing Symbiodinium cultures and corals to spectral light revealed different effects of blue and red light on the photosynthetic rhythm, specifically shortening or increasing the cycle time respectively. These findings suggest that the photosynthetic rhythm is entrained by different light cues, which are wired to an endogenous circadian clock. Furthermore, we provide evidence that mRNA expression was higher under blue light for two potential cryptochrome genes and higher under red light for a phytochrome gene isolated from Symbiodinium. These results offer the first evidence of the impact of the intensity and quality of light on the photosynthetic rhythm in algal cells living freely or as part of a symbiotic association. Our results indicate the presence of a circadian oscillator in Symbiodinium governing the photosynthetic apparatus through a light-induced signaling pathway that has yet to be described. 相似文献
4.
5.
André L. Mallet Claire E. Carver 《Journal of experimental marine biology and ecology》2009,374(2):128-133
One-year-old bay scallops, Argopecten irradians irradians (58 ± 2 mm, 22 ± 1 g live weight) were exposed to four replicated photoperiod treatments (24D, 8L:16D, 16L:8D, and 24L where D = dark hours, L = light hours) in order to measure the effect on gonad weight and maturation during the conditioning process. Results indicated that day-lengths of more than 8 h are necessary to promote gonad maturation in bay scallops. After 6 wk, the mean gonad weight for scallops in the 16-h and 24-h light regimes was similar at 0.6 ± 0.1 g dry weight compared to a mean of 0.2 ± 0.1 g dry weight for those in the 8-h and 0-h light regimes. Histological assessment indicated significantly more follicular tissue development in both the male and female portion of the gonad in the two longer photoperiod treatments. Overall, gamete maturity was highest for the scallops in the 16-h light regime; the incidence of mature eggs was 50% compared to 35% in the 24-h light regime, 20% in the 8-h light regime and 10% in the 0-h light regime. Assessment of feeding rates indicated no significant difference in algal cell consumption among treatments. Total dry tissue weight doubled over the 6-wk conditioning trial with no significant differences among treatments. One-year-old bay scallops appear to be non-responsive to conditions suitable for gonad maturation (i.e. appropriate temperature and food levels) unless they receive more than 8 h of light exposure. This finding has important implications for northern hatcheries which typically condition broodstock indoors during the early spring. 相似文献
6.
Entrainment experiments have been carried out with geographically widely separated populations of the sand beach isopod Eurydice pulchra Leach subjected to periods of simulated tidal agitation imposed concurrently with a 24-h light: dark (L: D) cycle. Circatidal swimming rhythms of greatest amplitude were induced when agitation was applied with the subjective timing, within the L: D cycle, of local spring high tides. This occurred in a normal L: D regime and also when the L: D regime was phase shifted through 90°. Animals previously maintained in constant darkness (D: D) and subsequently exposed to simulated tidal disturbance at various times in constant darkness were unable to modulate the amplitude of circatidal swimming activity. Isopods previously maintained in a normal L: D cycle and subsequently subjected to artificial tidal agitation in constant darkness were, however, able to modulate circatidal activity. This indicates that E. pulchra is capable of detecting tidal agitation and daily light cues and using them in conjunction with its circadian “clock” to modulate its endogenous circatidal rhythmicity. The free-running semilunar rhythm of swimming activity entrained only when the timing of agitation within the day/night cycle mimicked the pattern of local spring high tides. Agitation with the timing of neap high tides entrained no free-running circa-semilunar activity pattern. 相似文献
7.
8.
The light-harvesting complex (LHC) is an essential component in light energy capture and transduction to facilitate downstream photosynthetic reactions in plant and algal chloroplasts. The unicellular dinoflagellate alga Symbiodinium is an endosymbiont of cnidarian animals, including corals and sea anemones, and provides carbohydrates generated through photosynthesis to host animals. Although Symbiodinium possesses a unique LHC gene family, called chlorophyll a-chlorophyll c2-peridinin protein complex (acpPC), its genome-level diversity and evolutionary trajectories have not been investigated. Here, we describe a phylogenetic analysis revealing that many of the LHCs are encoded by highly duplicated genes with multi-subunit polyprotein structures in the nuclear genome of Symbiodinium minutum. This analysis provides an extended list of the LHC gene family in a single organism, including 80 loci encoding polyproteins composed of 145 LHC subunits recovered in the phylogenetic tree. In S. minutum, 5 phylogenetic groups of the Lhcf-type gene family, which is exclusively conserved in algae harboring secondary plastids of red algal origin, were identified. Moreover, 5 groups of the Lhcr-type gene family, of which members are known to be associated with PSI in red algal plastids and secondary plastids of red algal origin, were identified. Notably, members classified within a phylogenetic group of the Lhcf-type (group F1) are highly duplicated, which may explain the presence of an unusually large number of LHC genes in this species. Some gene units were homologous to other units within single loci of the polyprotein genes, whereas intergenic homologies between separate loci were conspicuous in other cases, implying that gene unit ‘shuffling’ by gene conversion and/or genome rearrangement might have been a driving force for diversification. These results suggest that vigorous intra- and intergenic gene duplication events have resulted in the genomic framework of photosynthesis in coral symbiont dinoflagellate algae. 相似文献
9.
Our understanding of reef corals and their fate in a changing climate is limited by our ability to monitor the diversity and abundance of the dinoflagellate endosymbionts that sustain them. This study combined two well-known methods in tandem: fluorescent in situ hybridization (FISH) for genotype-specific labeling of Symbiodinium and flow cytometry to quantify the abundance of each symbiont clade in a sample. This technique (FISH-Flow) was developed with cultured Symbiodinium representing four distinct clades (based on large subunit rDNA) and was used to distinguish and quantify these types with high efficiency and few false positives. This technique was also applied to freshly isolated symbionts of Orbicella faveolata and Orbicella annularis. Isolates from acutely bleached coral tissues had significantly lower labeling efficiency; however, isolates from healthy tissue had efficiencies comparable to cultured Symbiodinium trials. RNA degradation in bleaching samples may have interfered with labeling of cells. Nevertheless, we were able to determine that, with and without thermal stress, experimental columns of the coral O. annularis hosted a majority of clade B and B/C symbionts on the top and side of the coral column, respectively. We demonstrated that, for cultured Symbiodinium and Symbiodinium freshly isolated from healthy host tissues, the relative ratio of clades could be accurately determined for clades present at as low as 7 % relative abundance. While this method does not improve upon PCR-based techniques in identifying clades at background levels, FISH-Flow provides a high precision, flexible system for targeting, quantifying and isolating Symbiodinium genotypes of interest. 相似文献
10.
Colley NJ Trench RK 《Proceedings of the Royal Society of London. Series B, Containing papers of a Biological character. Royal Society (Great Britain)》1983,219(1214):61-82
We have investigated whether interactions between cell-surface macromolecules play a role in cellular recognition leading to specificity in the establishment of intracellular symbiosis between dinoflagellates and the polyp (scyphistoma) stage of the jellyfish Cassiopeia xamachana. All strains of the symbiotic dinoflagellate Symbiodinium microadriaticum were phagocytosed by the endodermal cells of the scyphistomae when presented to them as cells freshly isolated from their respective hosts. The rates of phagocytosis of such cells were high, and were directly correlated with the presence of a membrane, thought to be the host cell vacuolar membrane that surrounds the freshly isolated algae. Cultured algae lack this membrane. All cultured algae, even those that proliferate in host tissues, were phagocytosed at very low or undetectable rates. Freshly isolated algae treated with reagents that removed the host membrane were phagocytosed at low rates. The endodermal cells of the scyphistomae of the non-symbiotic medusa Aurelia aurita also phagocytosed freshly isolated algae, but did not phagocytose cultured algae. Phagocytosis of algae and carmine particles was found to be a competitive process in scyphistomae of C. xamachana. No correlation was observed between the surface electrical charge on algae and their phagocytosis by host endodermal cells. Neither was there any correlation between phagocytosis and persistence. We conclude that the specificity in symbioses between marine invertebrates and dinoflagellates appears to be regulated by processes that occur after potential algal symbionts are phagocytosed. 相似文献
11.
Buntora Pasaribu I-Ping Lin Jason T. C. Tzen Guang-Yuh Jauh Tung-Yung Fan Yu-Min Ju Jing-O Cheng Chii-Shiarng Chen Pei-Luen Jiang 《Marine biotechnology (New York, N.Y.)》2014,16(5):560-571
Intracellular lipid droplets (LDs) have been proposed to play a key role in the mutualistic endosymbiosis between reef-building corals and the dinoflagellate endosymbiont Symbiodinium spp. This study investigates and identifies LD proteins in Symbiodinium from Euphyllia glabrescens. Discontinuous Percoll gradient centrifugation was used to separate Symbiodinium cells from E. glabrescens tentacles. Furthermore, staining with a fluorescent probe, Nile red, indicated that lipids accumulated in that freshly isolated Symbiodinium cells and lipid analyses further showed polyunsaturated fatty acids (PUFA) was abundant. The stable LDs were purified from endosymbiotic Symbiodinium cells. The structural integrity of the Symbiodinium LDs was maintained via electronegative repulsion and steric hindrance possibly provided by their surface proteins. Protein extracts from the purified LDs revealed a major protein band with a molecular weight of 20 kDa, which was termed Symbiodinium lipid droplet protein (SLDP). Interestingly, immunological cross-recognition analysis revealed that SLDP was detected strongly by the anti-sesame and anti-cycad caleosin antibodies. It was suggested that the stable Symbiodinium LDs were sheltered by this unique structural protein and was suggested that SLDP might be homologous to caleosin to a certain extent. 相似文献
12.
J. C. Bythell A. E. Douglas V. A. Sharp J. B. Searle B. E. Brown 《Proceedings. Biological sciences / The Royal Society》1997,264(1386):1277-1282
As an approach to investigate the impact of solar radiation on an alga–invertebrate symbiosis, the genetic variation and photosynthetic responses of the dinoflagellate algal symbiosis in an intertidal and a subtidal population of the sea anemone Anemonia viridis were explored. Allozyme analysis of the anemones indicated that the two populations were genetically very similar, with a Nei''s index value of genetic identity (I) of 0.998. The algae in all animals examined were identified as Symbiodinium of clade a by PCR-RFLP analysis of the small subunit ribosomal RNA gene. The symbiosis in the two populations did not differ significantly in algal population density, chlorophyll a content per algal cell or any photosynthetic parameter obtained from studies of the relationship between photosynthesis and irradiance. We conclude that there is not necessarily genetic variation or photosynthetic plasticity of the symbiotic algae in Anemonia viridis inhabiting environments characterized by the different solar irradiances of the subtidal and intertidal habitats. 相似文献
13.
Intracellular pH (pHi) is likely to play a key role in maintaining the functional success of cnidarian–dinoflagellate symbiosis, yet until now the pHi of the symbiotic dinoflagellates (genus Symbiodinium) has never been quantified. Flow cytometry was used in conjunction with the ratiometric fluorescent dye BCECF to monitor changes in pHi over a daily light/dark cycle. The pHi of Symbiodinium type B1 freshly isolated from the model sea anemone Aiptasia pulchella was 7.25 ± 0.01 (mean ± SE) in the light and 7.10 ± 0.02 in the dark. A comparable effect of irradiance was seen across a variety of cultured Symbiodinium genotypes (types A1, B1, E1, E2, F1, and F5) which varied between pHi 7.21–7.39 in the light and 7.06–7.14 in the dark. Of note, there was a significant genotypic difference in pHi, irrespective of irradiance. 相似文献
14.
Lipid content and fatty acid profiles of corals and their dinoflagellate endosymbionts are known to vary in response to high-temperature stress. To better understand the heat-stress response in these symbionts, we investigated cultures of Symbiodinium goreauii type C1 and Symbiodinium sp. clade subtype D1 grown under a range of temperatures and durations. The predominant lipids produced by Symbiodinium are palmitic (C16) and stearic (C18) saturated fatty acids and their unsaturated analogs, the polyunsaturated fatty acid docosahexaenoic acid (C22:6, n-3; DHA), and a variety of sterols. Prolonged exposure to high temperature causes the relative amount of unsaturated acids within the C18 fatty acids in Symbiodinium tissue to decrease. Thermal stress also causes a decrease in abundance of fatty acids relative to sterols, as well as the more specific ratio of DHA to an algal 4-methyl sterol. These shifts in fatty acid unsaturation and fatty acid-to-sterol ratios are common to both types C1 and D1, but the apparent thermal threshold of lipid changes is lower for type C1. This work indicates that ratios among free fatty acids and sterols in Symbiodinium can be used as sensitive indicators of thermal stress. If the Symbiodinium lipid stress response is unchanged in hospite, the algal heat-stress biomarkers we have identified could be measured to detect thermal stress within the coral holobiont. These results provide new insights into the potential role of lipids in the overall Symbiodinium thermal stress response. 相似文献
15.
On coral reefs, Symbiodinium spp. are found in most cnidarian species, but reside in only a small number of sponge species. Of the sponges that do harbor Symbiodinium, most are found in the family Clionaidae, which represents a minor fraction of the poriferan diversity on a reef. Our goal was to determine whether Symbiodinium can be taken up by sponge hosts that do not typically harbor these algal symbionts, and then to follow the fate of any Symbiodinium that enter the intracellular space. We used the filter-feeding capacity of sponges to initiate intracellular interactions between sponge-specialist clade G Symbiodinium and six sponge species that do not associate with Symbiodinium. Using a pulse-chase experimental design, we determined that all of the species we examined captured Symbiodinium, and undamaged intracellular algae were found up to 1 h after inoculation. In a longer-term experiment, Symbiodinium populations in Amphimedon erina persisted in sponge cells for at least 5 d post-inoculation. While no evidence of digestion was detected, the population decreased exponentially after inoculation. We contrast these data with the characteristics of symbiont acquisition and establishment in Cliona varians, which normally harbors Symbiodinium. Explants from experimentally derived aposymbiotic sponges were placed in the field where they acquired Symbiodinium from ambient sources (i.e., we did not inoculate them as in the pulse-chase experiments). We began to detect Symbiodinium cells in C. varians after 12 d, and the algal population increased exponentially until densities approached those typically found in this host (after ~128 d). We discuss the implications of this work in light of growing interest in the evolution of specificity between hosts and symbionts, and the fundamental and realized niche of Symbiodinium. 相似文献
16.
Jing Jiang Hao Zhang Gregory S. Orf Yue Lu Wenxin Xu Lucas B. Harrington Haijun Liu Cynthia S. Lo Robert E. Blankenship 《BBA》2014
The chlorophyll a-chlorophyll c2-peridinin-protein (apcPC), a major light harvesting component in peridinin-containing dinoflagellates, is an integral membrane protein complex. We isolated functional acpPC from the dinoflagellate Symbiodinium. Both SDS-PAGE and electrospray ionization mass spectrometry (ESI-MS) analysis quantified the denatured subunit polypeptide molecular weight (MW) as 18 kDa. Size-exclusion chromatography (SEC) and blue native gel electrophoresis (BN-PAGE) were employed to estimate the size of native acpPC complex to be 64–66 kDa. We also performed native ESI-MS, which can volatilize and ionize active biological samples in their native states. Our result demonstrated that the native acpPC complex carried 14 to 16 positive charges, and the MW of acpPC with all the associated pigments was found to be 66.5 kDa. Based on these data and the pigment stoichiometry, we propose that the functional light harvesting state of acpPC is a trimer. Our bioinformatic analysis indicated that Symbiodinium acpPC shares high similarity to diatom fucoxanthin Chl a/c binding protein (FCP), which tends to form a trimer. Additionally, acpPC protein sequence variation was confirmed by de novo protein sequencing. Its sequence heterogeneity is also discussed in the context of Symbiodinium eco-physiological adaptations. 相似文献
17.
Daniel J. Thornhill Michael W. Daniel Gregory W. Schmidt 《Journal of experimental marine biology and ecology》2006,338(1):50-56
The ability to acquire different types of the symbiotic dinoflagellate Symbiodinium (zooxanthellae) from the environment was investigated using aposymbiotic scyphistomae of the jellyfish Cassiopea xamachana. Non-symbiotic scyphistomae were placed on an offshore Florida patch reef and in Florida Bay during 3- and 5-day periods in March, and 5-day exposures in May, August and December of 2003. Scyphistomae were maintained in culture for several months, after which members of clades A, B, C and D Symbiodinium were detected in these hosts by denaturing gradient gel electrophoresis (DGGE) analyses. These findings contrast with naturally collected C. xamachana medusa from Florida Bay where all specimens possessed only Symbiodinium type A1. Furthermore, the polyps did not acquire the symbionts found in nearby cnidarian colonies, suggesting that a diverse pool of symbiont lineages exists in the environment. These results support previous laboratory studies where aposymbiotic hosts were initially non-selective and capable of acquiring many kinds of Symbiodinium. The specificity seen in adult hosts is likely a result of post-infection processes due to competitive exclusion or other mechanisms. A higher percentage of polyps became infected after 5 days of exposure, compared to 3 days, and no infections were observed in laboratory controls held in filtered seawater. Infections were lowest (50% at both sites) in March of 2003, when seawater temperatures were at their annual minima. Infection was 100% in scyphistomae exposed for 5 days during the months of May, August and December of 2003. These findings suggest that this host system, in addition to addressing questions of host-symbiont selectivity, can be employed to monitor and define the abundance and distribution of natural pools of Symbiodinium. 相似文献
18.
Camila Granados-Cifuentes Joseph Neigel Paul Leberg Mauricio Rodriguez-Lanetty 《Coral reefs (Online)》2015,34(3):927-939
Although reef corals are dependent of the dinoflagellate Symbiodinium, the large majority of corals spawn gametes that do not contain their vital symbiont. This suggests the existence of a pool of Symbiodinium in the environment, of which surprisingly little is known. Reefs around Curaçao (Caribbean) were sampled for free-living Symbiodinium at three time periods (summer 2009, summer 2010, and winter 2010) to characterize different habitats (water column, coral rubble, sediment, the macroalgae Halimeda spp., Dictyota spp., and Lobophora variegata, and the seagrass Thalassia testudinum) that could serve as environmental sources of symbionts for corals. We detected the common clades of Symbiodinium that engage in symbiosis with Caribbean coral hosts A, B, and C using Symbiodinium-specific primers of the hypervariable region of the chloroplast 23S ribosomal DNA gene. We also discovered clade G and, for the first time in the Caribbean, the presence of free-living Symbiodinium clades F and H. Additionally, this study expands the habitat range of free-living Symbiodinium as environmental Symbiodinium was detected in T. testudinum seagrass beds. The patterns of association between free-living Symbiodinium types and habitats were shown to be complex. An interesting, strong association was seen between some clade A sequence types and sediment, suggesting that sediment could be a niche where clade A radiated from a free-living ancestor. Other interesting relationships were seen between sequence types of Symbiodinium clade C with Halimeda spp. and clades B and F with T. testudinium. These relationships highlight the importance of some macroalgae and seagrasses in hosting free-living Symbiodinium. Finally, studies spanning beyond a 1-yr cycle are needed to further expand on our results in order to better understand the variation of Symbiodinium in the environment through time. All together, results presented here showed that the great diversity of free-living Symbiodinium has a dynamic distribution across habitats and time. 相似文献
19.
The symbiosis between zooxanthellae (dinoflagellate genus Symbiodinium) and corals is a fundamental basis of tropical marine ecosystems. However the physiological interactions of the hosts and symbionts are poorly understood. Recently, intracellular crystalline deposits in Symbiodinium were revealed to be uric acid functioning for nutrient storage. This is the first exploration of these enigmatic crystalline materials that had previously been misidentified as oxalic acid, providing new insights into the nutritional strategies of Symbiodinium in oligotrophic tropical waters. However, we believe these deposits also function as eye-spots on the basis of light and electron microscopic observations of motile cells of cultured Symbiodinium. The cells possessed crystalline deposit clusters in rows with each row 100–150 nm thick corresponding to 1/4 the wavelength of light and making them suitable for maximum wave interference and reflection of light. Crystalline clusters in cells observed with a light microscope strongly refracted and polarized light, and reflected or absorbed short wavelength light. The facts that purines, including uric acid, have been identified as the main constituents of light reflectors in many organisms, and that the photoreceptor protein, opsin, was detected in our Symbiodinium strain, support the idea that uric acid deposits in Symbiodinium motile cells may function as a component of an eye-spot. 相似文献
20.
Summary The circadian rhythm of the photoresponse to blue light in the dinoflagellate Gyrodinium dorsum Kofoid was investigated by the use of a closed circuit television system. The initial cessation of movement upon stimulation (stop-response) was used as the index of light reception. Under constant dark conditions cells grown on a 12L:12D regime show an endogenous circadian rhythm in their stop-response with maximum responsiveness occurring approximately one hour before the beginning of the expected light phase. This rhythmic response was only observed if the cells were irradiated with red light (620 nm) prior to stimulation with blue light. After preirradiation both far-red reversibility and the shift in the stop-response action spectrum from 470 nm to 490 nm could also be demonstrated. These findings may be related to the diurnal migration of marine dinoflagellates.This study was supported by National Science Foundation grant GB 5137. 相似文献