Symbiosis and the Evolution of Larger Foraminifera

Lee, J. J.; McEnery, M. E.; Kahn, E. G.; Schuster, Frederick L.

doi:10.2307/1485262

Cited by 122 publications

(127 citation statements)

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“…Since investigations of multiple stressors on other marine organisms showed significant differences among taxa, the experiment included two species of Foraminifera. Heterostegina depressa and M. vertebralis represent two phylogenetically distinct clades that appear to have diverged [500 million years ago, evolved calcification independently of each other (Pawlowski et al 2003) and host different types of photosymbionts (Lee 2006).…”

Section: Introductionmentioning

confidence: 99%

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

2014

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Warming and changes in ocean carbonate chemistry alter marine coastal ecosystems at an accelerating pace. The interaction between these stressors has been the subject of recent studies on reef organisms such as corals, bryozoa, molluscs, and crustose coralline algae. Here we investigated the combined effects of elevated sea surface temperatures and pCO 2 on two species of photosymbiont-bearing coral reef Foraminifera: Heterostegina depressa (hosting diatoms) and Marginopora vertebralis (hosting dinoflagellates). The effects of single and combined stressors were studied by monitoring survivorship, growth, and physiological parameters, such as respiration, photochemistry (pulse amplitude modulation fluorometry and oxygen production), and chl a content. Specimens were exposed in flow-through aquaria for up to seven weeks to combinations of two pCO 2 (*790 and *490 latm) and two temperature (28 and 31°C) regimes. Elevated temperature had negative effects on the physiology of both species. Elevated pCO 2 had negative effects on growth and apparent photosynthetic rate in H.depressa but a positive effect on effective quantum yield. With increasing pCO 2 , chl a content decreased in H. depressa and increased in M. vertebralis. The strongest stress responses were observed when the two stressors acted in combination. An interaction term was statistically significant in half of the measured parameters. Further exploration revealed that 75 % of these cases showed a synergistic (= larger than additive) interaction between the two stressors. These results indicate that negative physiological effects on photosymbiont-bearing coral reef Foraminifera are likely to be stronger under simultaneous acidification and temperature rise than what would be expected from the effect of each of the stressors individually.

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Section: Introductionmentioning

confidence: 99%

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

2014

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“…The morphological characteristics of Symbiodinium symbionts isolated in culture from specimens of Sorites dominicensis collected from the Florida Keys have been described by Lee et al (1979Lee et al ( , 1997. Symbionts are distributed throughout the foraminiferal cytoplasm, with the highest densities occurring in the intermediate chambers and the lowest densities occurring in the outer chambers where the digestive vacuoles are concentrated (Richardson, 2006;Müller-Merz and Lee, 1976).…”

Section: S M I T H S O N I a N C O N T R I B U T I O N S T O T H E M mentioning

confidence: 99%

“…Sorites dominicensis Ehrenberg, 1839, is one of several living foraminiferal species that are host to algal endosymbionts (Hallock, 1999;Lee et al, 1979). Benthic foraminiferans with algal symbionts occur in several different clades (Soritacea, Alveolinacea, Nummulitacea, Calcarinidae, and Amphisteginidae) and are widely distributed in shallow-water, tropical to subtropical reef-associated marine ecosystems (Langer and Hottinger, 2000).…”

Section: Introductionmentioning

confidence: 99%

“…Although DNA sequences have not yet been obtained from the endosymbionts of either the Belizean or Indian River Lagoon populations of Sorites dominicensis, Symbiodinium sequences from Florida Keys specimens fall within either clade F (subclade F4) or H (Garcia-Cuetos et al, 2005;. In all phylogenies published to date, clade H, the dominant phylotype isolated from the Florida Keys, branches as the sister group to clade C, a clade that is widely distributed in the Indo-Pacifi c, and exhibits more sensitivity to bleaching than the other Symbiodinium clades (Garcia-Cuetos et al, 2005;Pawlowski et al 2001;Pochon et al, 2001Pochon et al, , 2004Rowan, 1998Rowan, , 2004.The morphological characteristics of Symbiodinium symbionts isolated in culture from specimens of Sorites dominicensis collected from the Florida Keys have been described by Lee et al (1979Lee et al ( , 1997. Symbionts are distributed throughout the foraminiferal cytoplasm, with the highest densities occurring in the intermediate chambers and the lowest densities occurring in the outer chambers where the digestive vacuoles are concentrated (Richardson, 2006;Müller-Merz and Lee, 1976).…”

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confidence: 99%

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Proceedings of the Smithsonian Marine Science Symposium

Lang¹,

Macintyre²,

Rützler³

2009

Smithsonian Contributions to the Marine Sciences

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s m i t h s o n i a n c o n t r i b u t i o n s t o t h e m a r i n e s c i e n c e s • n u m b e r 3 8 SERIES PUBLICATIONS OF THE SMITHSONIAN INSTITUTIONEmphasis upon publication as a means of "diffusing knowledge" was expressed by the fi rst Secretary of the Smithsonian. In his formal plan for the Institution, Joseph Henry outlined a program that included the following statement: "It is proposed to publish a series of reports, giving an account of the new discoveries in science, and of the changes made from year to year in all branches of knowledge." This theme of basic research has been adhered to through the years by thousands of titles issued in series publications under the Smithsonian imprint, commencing with Smithsonian Contributions to Knowledge in 1848 and continuing with the following active series: Smithsonian Contributions to Anthropology Smithsonian Contributions to Botany Smithsonian Contributions in History and Technology Smithsonian Contributions to the Marine Sciences Smithsonian Contributions to Museum Conservation Smithsonian Contributions to Paleobiology Smithsonian Contributions to ZoologyIn these series, the Institution publishes small papers and full-scale monographs that report on the research and collections of its various museums and bureaus. The Smithsonian Contributions Series are distributed via mailing lists to libraries, universities, and similar institutions throughout the world.Manuscripts submitted for series publication are received by the Smithsonian Institution Scholarly Press from authors with direct affi liation with the various Smithsonian museums or bureaus and are subject to peer review and review for compliance with manuscript preparation guidelines. General requirements for manuscript preparation are on the inside back cover of printed volumes. For detailed submissions requirements and to review the "Manuscript Preparation and Style Guide for Authors," visit the Submissions page at www.scholarlypress.si.edu. The paper used in this publication meets the minimum requirements of the American National Standard for Permanence of Paper for Printed Library Materials Z39. Foreword N early two-thirds of Earth's surface is covered by the ocean, a global system essential to all life. Impacts on one part of the ocean can have worldwide effects. The ocean moderates our climate, provides valuable resources, and produces at least half the oxygen we breathe: it makes our planet livable. We know little, however, about the physical, chemical, geological, and biological aspects of this crucial life support system. s m i t h s o n i a n c o n t r i b u t i o n s t o t h e m a r i n S M I T H S O N I A N C O N T R I B U T I O N S T O T H E M A R I N E S C I E N C E S MARINE BIODIVERSITY, EVOLUTION, AND SPECIATION S M I T H S O N I A N C O N T R I B U T I O N S T O T H E M A R I N E S C I E N C E S i i i • S M I T H S O N I A N C O N T R I B U T I O N S T O T H E M A R I N E S C I E N C E SThe Smithsonian Institution, in efforts to increase knowledge about the ocean, has established a ...

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“…M. vertebralis forms a symbiotic partnership with one of the most important symbiotic algal species in tropical reef systems, the dinoflagellate Symbiodinium (Pawlowski et al, 2001), renowned for living in endosymbioses with reefbuilding corals across the globe (Baker, 2003). This partnership has evolved to make use of the abundance of light in the clear, nutrient-poor waters of the reef; whereby the host receives energy from the photosynthetic symbiont in the form of fixed carbon (Lee, 2006) in exchange for providing the symbiont with access to a rich supply of inorganic nutrients. Although light underpins the health and function of coral reef ecosystems, in excess, light can result in reduced photosynthetic efficiency, and if not protected against, damage to the photosynthetic machinery of the symbiont can ensue (Brown et al, 1999;Jones and Hoegh-Guldberg, 2001).…”

Section: Introductionmentioning

confidence: 99%

A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera

2016

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Light underpins the health and function of coral reef ecosystems, where symbiotic partnerships with photosynthetic algae constitute the life support system of the reef. Decades of research have given us detailed knowledge of the photoprotective capacity of phototrophic organisms, yet little is known about the role of the host in providing photoprotection in symbiotic systems. Here we show that the intracellular symbionts within the large photosymbiotic foraminifera Marginopora vertebralis exhibit phototactic behaviour, and that the phototactic movement of the symbionts is accomplished by the host, through rapid actin-mediated relocation of the symbionts deeper into the cavities within the calcium carbonate test. Using a photosynthetic inhibitor, we identified that the infochemical signalling for host regulation is photosynthetically derived, highlighting the presence of an intimate communication between the symbiont and the host. Our results emphasise the central importance of the host in photosymbiotic photoprotection via a new mechanism in foraminifera that can serve as a platform for exploring host-symbiont communication in other photosymbiotic organisms.

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Symbiosis and the Evolution of Larger Foraminifera

Cited by 122 publications

References 43 publications

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

Proceedings of the Smithsonian Marine Science Symposium

A novel mechanism for host-mediated photoprotection in endosymbiotic foraminifera

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