Buried alive – germination of up to a century-old marine protist resting stages

Lundholm, Nina; Ribeiro, Sofia; Andersen, Thorbjørn Joest; Koch, Trine; Godhe, Anna; Ekelund, Flemming; Ellegaard, Marianne

doi:10.2216/11-16.1

Cited by 100 publications

(92 citation statements)

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“…In polar areas also, many phototrophic organisms routinely survive periods of several months in the dark during the long polar winter. Perhaps the longest periods of darkness that have been endured by phototrophs are those experienced by some algal cysts or spores, examples of which have germinated after more than a century in darkness (figure 1) [1].…”

Section: Introductionmentioning

confidence: 99%

Dark survival in a warming world

McMinn

Martin

2013

Proc. R. Soc. B.

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Most algae regularly experience periods of darkness ranging from a few hours to a few days. During this time, they are unable to photosynthesize, and so must consume stored energy products. However, some organisms such as polar algae and some microalgal cysts and spores are exposed to darkness for months to years, and these must use alternative strategies to survive. Some taxa, such as dinoflagellates, form cysts and become dormant. Others use physiological methods or adopt mixotrophy. The longest documented survival of more than a century was for dinoflagellates buried in sediments in a Norwegian fjord. Seasonal changes in daylight hours are naturally unaffected by climate change. This means that polar microalgae will in the future need to survive the same period of seasonal darkness but at higher temperatures, and this will require a greater drawdown of stored energy. Recent experimental work has shown that both Arctic and Antarctic phytoplankton are able to survive increases of up to 6°C in the dark.

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Section: Introductionmentioning

confidence: 99%

Dark survival in a warming world

McMinn

Martin

2013

Proc. R. Soc. B.

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“…and 1922 (+12 years s.e.) [9,10], representing changes in population composition over approximately a century (84 + 12 years s.e. ); these slices yielded 41, 31, 33 and 29 clonal strains, respectively, with each strain representing a single haploid cell isolated from a cell culture of a germinated cyst.…”

Section: Methodsmentioning

confidence: 99%

“…Protist cysts may remain viable for up to 100 years [9,10], thereby providing a source of naturally archived historic material. We revived cysts of Pentapharsodinium dalei, a spring-blooming marine dinoflagellate that inhabits polar, sub-polar and coldtemperate coastal regions, from samples spanning some 100 years to make the first estimates of contemporary N e in a free-living protist population.…”

Section: Introductionmentioning

confidence: 99%

“…Nonetheless, for protists that can be genotyped at many loci and during a diploid phase, single sample estimators of N e could also be used [22]. For most protists, however, there remains an apparent need for temporally separated samples to obtain accurate estimates of N e , and this should not present a major obstacle for species that produce cysts as they are amenable to the palaeogenetic approach used here (see also [9,10,23]). …”

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confidence: 99%

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A century-long genetic record reveals that protist effective population sizes are comparable to those of macroscopic species

et al. 2013

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Effective population size (N e ) determines the rate of genetic drift and the relative influence of selection over random genetic changes. While free-living protist populations characteristically consist of huge numbers of cells (N), the absence of any estimates of contemporary N e raises the question whether protist effective population sizes are comparably large. Using microsatellite genotype data of strains derived from revived cysts of the marine dinoflagellate Pentapharsodinium dalei from sections of a sediment record that spanned some 100 years, we present the first estimates of contemporary N e for a local population in a free-living protist. The estimates of N e are relatively small, of the order of a few 100 individuals, and thus are similar in magnitude to values of N e reported for multicellular animals: the implications are that N e of P. dalei is of many orders of magnitude lower than the number of cells present (N e /N 10 212 ) and that stochastic genetic processes may be more prevalent in protist populations than previously anticipated.

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“…Other genera of dinoflagellates are well known for their ability to persist for extended periods of time within sediment (Lewis et al 1999) and it is possible that Symbiodinium may similarly persist in this habitat. Benthic-pelagic coupling in dinoflagellates has been observed in cells vertically migrating into sediment (Sinclair and Kamykowski 2008), and also through the encystment and long term burial of cells that are viable up to after 100 years of dormancy (Lundholm et al 2011). While most photosynthetic organisms experience periods of darkness on a daily basis, microalgae that associate with sediment may experience dark periods of days to weeks, or even longer (McMinn and Martin 2013).…”

Section: Introductionmentioning

confidence: 99%

The free-living Symbiodinium reservoir and scleractinian coral symbiont acquisition

Nitschke¹

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The genus Symbiodinium (Dinophyceae, Suessiales), a group of geographically widespread marine dinoflagellates, comprises numerous ecologically and genetically distinct taxa. Symbiodinium spp.establish intracellular symbioses with cnidarians, infecting hosts such as jellyfish, sea anemones, octocorals and reef-building corals. The energetic demands of hosts can be met at varying levels by Symbiodinium through translocation of photosynthetically-fixed carbon, assisting in the formation of coral reefs. The cnidarian-dinoflagellate symbiosis is relatively well studied. In contrast, empirical data for population dynamics, distribution, and physiology of free-living Symbiodinium are limited.Therefore this thesis aims to characterise the dynamics between free-living Symbiodinium cells, hosts, and their habitat.Free-living Symbiodinium cells have been identified in reef sediment, and this study investigated whether adult coral colonies are a significant source of benthic Symbiodinium cells. Acropora millepora colonies were translocated to bare patches of sediment (Heron Reef, Great Barrier Reef, Australia), and the surrounding sediment was sampled for Symbiodinium cells over a period of 18 months. An 8-fold increase in visually-identified cells relative to the background population was recorded from the sediment at the immediate base of coral colonies. Symbiodinium abundance returned to background levels after the removal of the coral. These fine-scale changes in the distribution of cells suggests that hard-coral may be an important 'passive' source of Symbiodinium.The 'active' supply of Symbiodinium cells to the benthos was investigated through direct contact of coral tissue with sediment. Symbiont loss was induced in the coral Pocillopora damicornis through burial of coral branches. Peak cell abundance in the sediment occurred after four days, but the photophysiology (F v /F m ) of the Symbiodinium cells was significantly impaired. By day 12, Symbiodinium cells were present only in low concentrations in sediment samples, and the majority of cells were substantially degraded. In this study, Symbiodinium appeared to survive only transiently following expulsion, with an approximate window of viability of seven days. Such a period may be sufficient for coral recruits to make contact with potential symbionts in situ.Elevated temperatures induce a range of serious, deleterious effects in Symbiodinium. The potential amelioration of these effects was investigated, testing the hypothesis that Symbiodinium cells find refuge from stress when cultured within sediment. An exclusively free-living clade A (not known to form symbioses) and the symbiosis-forming type A1 were grown with or without a microhabitat of carbonate sediment at 25°C, 28°C or 31°C. The exclusively free-living clade A was physiologically superior to symbiosis-forming A1 across all measured variables and treatment combinations: it iii reproduced faster within the sediment, exhibited high levels of motility and maintained a stable maximum quantum yield (F ...

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Buried alive – germination of up to a century-old marine protist resting stages

Cited by 100 publications

References 50 publications

Dark survival in a warming world

Dark survival in a warming world

A century-long genetic record reveals that protist effective population sizes are comparable to those of macroscopic species

The free-living Symbiodinium reservoir and scleractinian coral symbiont acquisition

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