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2013 deGoeij Science Sponge loop

  • NIOZ Royal Netherlands Institute for Sea Research, and Utrecht University
DOI: 10.1126/science.1241981
, 108 (2013);342 Science
et al.Jasper M. de Goeij
Within Coral Reefs
Surviving in a Marine Desert: The Sponge Loop Retains Resources
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effects between duplicates. Although in some
cases, this interference can be exploited, for
example, by using it to repress gene expres-
sion (5,23), we propose that a more common
outcome is the minimization of this interfer-
ence in gene duplicates that persist over evo-
lutionary time. Whether such minimization is
generally accompanied by an increase in regu-
latory complexity, as seen here, remains to be
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24. Single-letter abbreviations for the amino acid
residues are as follows: A, Ala; C, Cys; D, Asp; E, Glu;
F, Phe; G, Gly; H, His; I, Ile; K, Lys; L, Leu; M, Met;
N, Asn; P, Pro; Q, Gln; R, Arg; S, Ser; T, Thr; V, Val;
W, Trp; and Y, Tyr.
Acknowledgments: We thank B. Tuch for assistance and
comments; O. Homann for assistance on experimental
techniques; and C. Nobile, C. Dalal, S. Devika, R. Bennett,
L. Mera, and T. Sorrells for comments. This work was funded
by grant RO1 GM057049 from the NIH.
Supplementary Materials
Materials and Methods
Figs. S1 to S4
Tables S1 to S5
References (2538)
21 May 2013; accepted 6 September 2013
Surviving in a Marine Desert: The
Sponge Loop Retains Resources
Within Coral Reefs
Jasper M. de Goeij,
*Dick van Oevelen,
Mark J. A. Vermeij,
Ronald Osinga,
Jack J. Middelburg,
Anton F. P. M. de Goeij,
Wim Admiraal
Ever since Darwinsearlydescriptionsofcoralreefs,scientistshavedebatedhowoneofthe
It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced
on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to
fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna.
This sponge loopwas confirmed in aquarium and in situ food web experiments, using
C- and
N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as
coral reefs persist in oligotrophic seasthe reefsparadoxand has implications for reef
ecosystem functioning and conservation strategies.
Coral reefs thrive in oligotrophic tropical
seas, but nevertheless belong to the most
productive ecosystems on Earth (13).
Efficient retention and recycling of carbon and
nutrients causes the net production of reefs to
be close to zero, despite high gross primary pro-
duction (4). Reef primary producers such as
corals and algae release up to 50% of their
fixed carbon (5,6), of which up to 80% im-
mediately dissolves in seawater (7). This shunt
into the dissolved organic matter (DOM) pool
represents a major flow of energy and nutrients
on coral reefs (7). In the open ocean, microbes
enable the transfer of DOM to higher trophic
levels through the well-established microbial
loop (8). Studies on coral reefs have therefore
also initially focused on microbes in reef waters
and adjacent permeable sediments to understand
the fate of DOM in these systems (7,911).
However, uptake rates by bacterioplankton, in
the sense of the microbial loop, are largely in-
sufficient to explain the observed DOM removal
on Caribbean and Indo-Pacific reefs (12). It there-
fore remains unclear how the largest source of
energy and nutrients on reefs is transferred to
higher trophic levels.
Cryptic habitats, for example, the coral reefs
crevices and cavities, are identified as major
sinks of DOM on Caribbean and Indo-Pacific
reefs (12). These habitats cover up to two-thirds
of the reefsvolume,andthebiomassofcryp-
tic organisms can exceed that on the open reef
(13,14). DOM removal rates in cryptic habitats
on Caribbean reefs (12) are comparable to the
average gross primary production rates of the
entire coral reef ecosystem (2). DOM removal
rates on Indo-Pacific reefs are lower (12)but
still account for up to 46% of the average gross
reef productivity. Sponges are primarily respon-
sible for total DOM uptake and remove the
same amount of DOM from the water column in
30 min as free-living bacteria take up in 30 days
(12,15). Therefore, sponges retain organic mat-
ter within the reef community and thereby pre-
vent energy and nutrient losses to the open ocean.
Surprisingly however, sponges respire only 42%
of the carbon taken up from the surrounding
water (15,16). Assuming that the remaining 58%
is used for growth, a biomass increase of 38% of
body carbon per day (more than a doubling of
biomass every 3 days) would be expected (16). In
reality, however, the net growth rate of sponges is
near zero (15,16), implying high losses of sponge
biomass through a rapid tissue turnover.
cells to the surrounding water has been shown
for the sponge Halisarca caerulea (17).The
5 to 6 hours, representing the fastest cell cycle
found in any multicellular organism to date (17).
This rapid cell production is counterbalanced by
massive shedding of old choanocytes as partic-
ulate organic matter (POM or detritus) into the
water column (17). Massive shedding of POM is
also observed in other tropical sponges (18,19).
Department of Aquat ic Ecology and Ecotoxicology, Instit ute for
Biodiversity and Ecosystem Dynamics, University of Amsterdam,
Post Office Box 94248, 1090 GE Amsterdam, Netherlands.
Department of Ecosystem Studies, NIOZ Royal Netherlands
Institute for Sea Research, NL-4400 AC Yerseke, Netherlands.
Department of Aquatic Microbiology,Institute for Biodiversity
and Ecosystem Dynamics, University of Amsterdam, Carmabi,
Piscaderabaai z/n Willemstad, Curaçao.
Department of Aqua-
culture and Fisheries, Wageningen University, Post OfficeBox
338, 6700 AH Wageningen, Netherlands.
Faculty of Geo-
sciences, Utrecht University, Budapestlaan 4, 3584 CD Utrecht,
Faculty of Health, Medicine and Life Sciences,
Maastricht University, Post Office Box 616, 6200 MD Maastricht,
*Corresponding author. E-mail:
4 OCTOBER 2013 VOL 342 SCIENCE www.sciencemag.org108
This suggests that sponges use the majority of
incorporated carbon to rejuvenate their filter sys-
tem and maintain a high cell turnover.
We hy p othe s ize he r e tha t s h ed sp o n ge ce l l s
(detritus) are subsequently ingested by particle-
feeding organisms (detritivores). Sponges thereby
make the energy and nutrients stored in the DOM
pool available to organisms at higher trophic lev-
els that would otherwise be unable to capitalize
on this resource. Because small detritivores (such
as crustaceans and polychaetes) are themselves
fed upon by larger animals higher in the food
web, sponges are at the base of a sponge loop that
ultimately recycles energy and nutrients back into
the ecosystem in a similar way as the microbial
loop does in the open ocean.
To st udy th e prop o sed D O M-s pong e-de t rit u s
feedback loop on coral reefs, we tested three key
predictions of this hypothesis: (i) sponges take up
DOM, (ii) sponges convert DOM into detritus,
and (iii) sponge-derived detritus is taken up by
detritivores. These three predictions were first
tested in flow chambers in a controlled running-
seawater aquarium setup (fig. S1) using
C- and
N-enriched DOM, extracted from the cosmo-
politan marine diatom Phaeodactylum tricornutum,
as a food web tracer (20).
All three key elements were confirmed ex-
perimentally (Fig. 1). Four common reef sponge
species showed uptake of dissolved organic car-
bon (DO
C) and nitrogen (DO
N) (Fig. 1A).
All four species subsequently produced
C- and
N-enriched detritus (Fig. 1B). The four sponge
species converted 11 to 24% of the assimilated
C) and 18 to 36% of
the DO
and B). Control incubations showed that detritus
production without sponges was less than 4%
of the detritus production in incubations with
sponges. Detritivores subsequently fed on the
labeled sponge-derived detritus (Fig. 1C). Iso-
topically enriched detritus, collected from speci-
mens of the four tested sponge species (fig. S2)
that were repeatedly fed with
C- and
DOM (20), was added to six cores containing cav-
ity sediments with residing fauna and, in three out
of six cores, motile fauna were added (hermit
crabs and snails) (fig. S1). Within 6 hours, sponge
detritus was incorporated by 17 out of 28 (
C) and
23 out of 28 (
N) specimens of detritivores.
After experimental confirmation of a sponge
loop in flow chambers, the question arose wheth-
er this newly found pathway could actually be
identified in a complex coral reef environment.
Therefore, the water exchange of two in situ
cryptic reef cavities (75 and 100 liters) with the
surrounding reef water was temporarily restricted
(12,20), and
C- and
N-enriched DOM was
injected into the enclosed cavity at the start of
two consecutive incubation periods of 3 hours
(fig. S3). Once we restored the water exchange
between the water column and the cavities, the
presence and fate of labeled DOM were ana-
lyzed over the subsequent 45 hours within the
main cavity compartments; that is, sponges,
sponge-derived detritus, surface sediment, bac-
terioplankton, nonsponge filter feeders, and mo-
tile fauna such as hermit crabs and snails (20).
The relative abundance of
compartments over time provided qualitative
Fig. 1. Fate of DOM tracer
bars) through sponge-
driven DOM transfer in flow
chamber experiments. (A)
Uptake of tracer DOM (DO
and DO
N; micromoles of
tracer per millimole of sponge
CorNTSD; n=4speci-
mens) by the sponge species
Halisarca caerulea (Hc), Hal-
iclona implexiformis (Hi),
Chondrilla caribensis (Cc),
and Scopalina ruetzleri (Sr).
The uptake of DO
sponges is further specified
in tissue assimilation (dark
red bars) and respiration
(light red bars). (B)Produc-
tion of detritus (PO
N; micromoles of tracer
per millimole of sponge C or
NTSD; n=4specimens)
by the sponges HC, HI, CC,
and SR. (C)Uptakeof
sponge-derived tracer detritus
N; micro-
moles of tracer per millimole
of faunal C or N TSD) by
detritivores (n=28speci-
mens) picked from six cores
of reef sediment; three cores
were supplemented with hermit crabs and snails.
Fig. 2. In situ sponge-
driven transfer of tracer
DOM (red line,
C; blue
N) in coral reef cav-
ities after a temporary
6-hour closure (gray shad-
ing) and the subsequent
45 hours. The mean above-
background isotope tracer incor-
poration (Dd
Cand Dd
of two cavities is shown for the com-
partments (A)sponges,(B)sponge-
derived detritus, and (C)detritivores;
that is, nonsponge filter feeders (solid
line) and motile fauna (dashed line). For guidance,
the interval of peak tracer incorporation is high-
lighted for each compartment. t,time;h,hours. SCIENCE VOL 342 4 OCTOBER 2013 109
evidence in support of our proposed pathway of
sponge-driven DOM transfer (Fig. 2). After the
introduction of labeled DOM to coral cavities, the
uptake of tracer
N was first observed
in sponges (first prediction: DOM-sponge; mean
sponge Dd
Fig. 2A) immediately after the 6-hour incubation
period. Between 12 and 24 hours after the in-
cubation, the relative isotope abundance peaked
in sponge-derived detritus (second prediction:
sponge-detritus; mean detritus Dd
tritus was finally transferred into motile fauna
and nonsponge filter feeders after 45 hours (third
prediction: detritushigher trophic levels; steady
increase to a detritivore Dd
C3to4and Dd
12 to 17;Fig.2C).The
derived detritus was lower than the
the sponges (Fig. 2, A and B), indicating that
the detritus was relatively enriched in N. The
DOM-derived Dd
N in the surface
sediment or the bacterioplankton was generally
lower than 2, indicating limited uptake by
these compartments.
The seemingly paradoxical observation that
productive ecosystems such as coral reefs thrive
in nutrient-poor waters can only be explained
through processes ensuring efficient capture, re-
tention, and recycling of energy and nutrients.
Such tight recycling mechanisms involve micro-
bial processing of coral- and algal-derived DOM
in the water column and permeable reef sands
(7,11). Here we show that, in addition to the
transfer of DOM via bacteria to fauna (8), sponges
transform the majority of DOM into particulate
detritus, a pathway that has hitherto not been
recognized (Fig. 3). The underlying mechanisms
of DOM uptake and rapid cell turnover in sponges
are not yet fully understood. Sponges form close
associations with microorganisms, forming so-
called holobionts, and both sponge cells and mi-
crobes can assimilate DOM (16), although their
relative contributions remain largely unknown.
The sponge loop nevertheless greatly enhances
our growing understanding of the efficiency that
typifies coral reefs, thus supporting reef life, in-
creasing biodiversity (21,22,)andmaintaining
high productivity. Sponges not only recycle the
energy retained in DOM but also provide reef
fauna with a source of nutrients (such as N),
thereby fertilizing the coral reef ecosystem. The
efficient and fast uptake, retention, and release
ecosystem by sponges may also catalyze nutrient-
induced shifts in the coral-algal-microbe com-
munity after eutrophication, often associated
with coral reef degradation (24,25). Top-down
controlled shifts from coral- to sponge-dominated
reefs have been predicted (26)andrecordedin
the Caribbean (27,28), but still sponges are rarely
considered in analyses of alternative stable states
on coral reefs. Other oligotrophic ecosystems where
sponges are abundant, such as deep-sea cold-water
coral reefs and temperate Mediterranean reefs,
may also sustain the functioning of a sponge loop.
Deep-sea sponges contribute substantially to the
respiration of cold-water reef communities (29)
and produce large amounts of detritus (30). Medi-
terranean reefs are dominated by (cryptic) sponges,
of which several abundant species are found to
take up DOM (31). Although this study shows
the presence of the sponge loop mainly qualita-
tively, DOM turnover by sponges (15)approaches
the daily gross primary production of the entire
reef ecosystem (2,4), suggesting that this ener-
getic pathway is of great ecological importance
(Fig. 3). Recognition of the key role of sponges in
coral reefs has, consequently, implications for
studies on ecosystem services and conservation
strategies in ecosystems where sponges are a
ubiquitous component.
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Acknowledgments: J.M.d.G. and D.v.O. contributed equally
to this work. We thank D. M. de Bakker, C .G. W. Whalen, and
B. E. Alexander for their technical assistance in the field
and lab; C. E. Mueller, and P. van Rijswijk for preparation of
the DOM substrate, lab assistance, and isotope analysis; and
E. R. Hunting for discussion. This work was supported
financially by the Innovational Research Incentives Scheme
of the Netherlands Organization for Scientific Research
(NWO-VENI; 863.10.009, granted to J.M.d.G.) and the
Schure-Beijerinck-Popping fund. J.M.d.G. and R.O. are also
affiliated with Porifarma BV Poelbos 3, 6718 HT Ede,
Netherlands. The authors declare no conflicts of interest.
A detailed description of all materials and methods and
additional data are available as supplementary materials.
All authors discussed the experimental data and jointly
wrote the manuscript. The data are deposited in DRYAD,
accession no.
Supplementary Materials
Materials and Methods
Figs. S1 to S3
References (3239)
17 June 2013; accepted 6 September 2013
Fig. 3. A simplified scheme of dominant pathways (millimoles of C m
transfer on coral reefs in the pelagic (blue), benthic reef (green), and sediment (yellow) eco-
system compartments. The proposed sponge loop (red arrow) is shown in addition to the classical mi-
crobial loop. GPP, gross primary production. *(2),(5,6), (7), (12), §(11,12(11); see (20)fordetails.
ResearchGate has not been able to resolve any citations for this publication.
Full-text available
We present a quantitative food-web analysis of the cold-water coral community, i.e., the assembly of living corals, dead coral branches and sediment beneath, associated with the reef-building Lophelia pertusa on the giant carbonate mounds at similar to 800-m depth at Rockall Bank. Carbon flows, 140 flows among 20 biotic and abiotic compartments, were reconstructed using linear inverse modeling by merging data on biomass, on-board respiration, delta(15)N values, and literature constraints on assimilation and growth efficiencies. The carbon flux to the coral community was 75.1 mmol C m(-2) d(-1) and was partitioned among (phyto) detritus (81%) and zooplankton (19%). Carbon ingestion by the living coral was only 9% of the carbon ingestion by the whole community and was portioned among (phyto) detritus (72%) and zooplankton (28%). Carbon cycling in the community was dominated by suspension- and filter-feeding macrofauna associated with dead coral branches. Sediment traps mounted on a bottom lander trapped 0.77 mmol C m(-2) d(-1) ( annual average), which is almost two orders of magnitude lower than total carbon ingestion (75.1) and respiration (57.3 mmol C m(-2) d(-1)) by the coral community. This discrepancy is explained in two ways: the coral community intercepts organic matter that would otherwise not settle on the seafloor, and through their action as ecosystem engineers, the increased turbulence generated by the coral framework and organic-matter depletion in the boundary layer augment the influx to the coral community. A comparison of macrofaunal biomass and respiration data with soft sediments reveals that coral communities are hot spots of biomass and carbon cycling along continental margins.
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Whenever actively photosynthesizing cells are exposed to conditions where carbon fluxes exceed intakes of other essential-nutrients required for formation of new biomass, cell division is arrested, and the excess carbon is stored, excreted or directed to secondary functions. The extent of this uncoupling and its’ implications in aquatic systems are discussed. We focus on three examples: the cellular level of free living phytoplankton, the ecosystem level in the microbial food web, and the highly specialized level of species interactions in the symbiotic association between zooxanthellae and corals. These examples highlight the adaptive significance of uncoupling between photosynthesis and growth in aquatic systems. Moreover, we underscore the fact that in many real-world situations, net primary productivity cannot be equated to population growth. Roles of the “excess” carbon include photoprotective pigments and buoyancy regulating ballast. The excreted carbon compounds may protect cells or cell masses from desiccation, and fuel the microbial loop. The microbial loop increases overall nutrient extraction efficiency compared to that of which phytoplankton alone are capable. The zooxanthellae-coelenterate symbiosis drives the nutrient and energy fluxes supporting coral reef life in the nutrient-poor tropical seas. In those mutualistic associations, since photosynthesis is normally uncoupled from cell growth, the algae excrete most of their photosynthate and that supports the metabolic activities of the host.
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The structure of Caribbean coral reef communities has been altered by numerous anthropogenic and natural stressors. Demographic studies of key functional groups have furthered efforts to describe and understand these changes. Little is known, however, about the demographics of sponges on coral reefs, despite their abundance and the important functions they perform (e.g., increased habitat complexity, water filtration). We have monitored permanent plots on reefs off Key Largo, Florida, USA, to study the demography of a particularly important species, the giant barrel sponge, Xestospongia muta. From 2000 to 2006, population densities of X. muta significantly increased at sites on Conch Reef by a mean of 46% (range = 16-108%) and on Pickles Reef by a mean of 33%. In 2006, densities of X. muta on Conch Reef ranged from 0.134 to 0.277 sponges/m2, and mean sponge volume was 1488 cm3/m2, with the largest size class of sponges constituting 75% of the total volume. Increased population density resulted from a significant increase in the number of sponges in the smallest size class. Recruit survival did not significantly change through time; however, a significant interaction between season and year on recruitment suggests that large recruitment pulses are driving population increases. Mean yearly recruitment rates ranged from 0.011 to 0.025 recruits x m(-2) x yr(-1), with pulses as high as 0.036 recruits/m2. To explore the demographic processes behind the population increase and determine future population growth of X. muta under present reef conditions, a stage-based matrix modeling approach was used. Variable recruitment pulses and mortality events were hypothesized to be large determinants of the demographic patterns observed for X. muta. Elasticity and life table response analysis revealed that survival of individuals in the largest size class has the greatest effect on population growth. Projections indicate that populations of X. muta will continue to increase under present conditions; however population growth may be negatively affected by continued mortality of the largest individuals from a recently described pathogenic syndrome.
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ARGRI, ARGRII, and ARGRIII proteins regulate the expression of arginine anabolic and catabolic genes. The integrity of these three proteins is required to observe the formation of a DNA-protein complex with the different promoters of arginine coregulated genes. A study of deletions and point mutations created in the 5' noncoding region of ARG3, ARG5,6, CAR1, and CAR2 genes shows that at least two regions, called BoxA and BoxB, are required for proper regulation of these genes by arginine and ARGR proteins. By gel retardation assay and DNase I footprinting analysis, we have determined precisely the target of the ARGR proteins. Sequences in and around BoxA are necessary for ARGR binding to these four promoters in vitro, whereas sequences in and around BoxB are clearly protected against DNase I digestion only for CAR1. Sequences present at BoxA and BoxB are well conserved among the four promoters. Moreover, pairing can occur between sequences at BoxA and BoxB which could lead to the creation of secondary structures in ARG3, ARG5,6, CAR1, and CAR2 promoters, favoring the binding of ARGR proteins in vivo.
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ARGRI, ARGRII, and ARGRIII regulatory proteins control the expression of arginine anabolic and catabolic genes in Saccharomyces cerevisiae. We have shown that MCM1 is part of the ARGR regulatory complex, by in vitro binding experiments, at the ARGR5,6 promoter. The participation of MCM1 in the regulation of arginine metabolism is confirmed by the behavior of an mcm1-gcn4 mutant, which is affected in the repression of arginine anabolic genes. In this mcm1 mutant, synthesis of the catabolic enzymes is rather constitutive, but this derepression requires the integrity of the ARGR system and of the target sequences of these proteins in the CAR1 promoter. Our in vitro binding experiments confirm the presence of MCM1 in the protein complex interacting with the promoters of the catabolic CAR1 and CAR2 genes. This is the first in vivo transcription role ascribed to MCM1 other than its role in the transcription of cell-type-specific genes.
We measured ammonium and nitrate plus nitrite fluxes from 14 common sponge species on a Florida Keys reef (Conch Reef) using a combination of incubation experiments and an in situ method that requires no manipulation of the sponge. On a 600-m² section of Conch Reef, species-specific biomass for all nonencrusting sponges was measured. The biomass data combined with species-specific dissolved inorganic nitrogen (DIN) flux rates yielded the benthic DIN flux from 14 species, and allowed us to extrapolate these data to the total nonencrusting sponge community. The species for which we measured DIN fluxes represented 85% of the nonencrusting sponge biomass in the study area and released a combined 480 ± 93 micromol m⁻²h⁻₁ of nitrate plus nitrite, and 57 ± 73 micromol m⁻²h⁻₁ of ammonium. Approximately 73% of the measured DIN flux was produced by Xestospongia muta, a massive barrel sponge. Of the 14 species studied, 10 hosted active nitrifying communities, and 8 hosted photosynthetic microbial associates. However, the presence of these microbial communities had no apparent effect on the magnitude of the total DIN flux. We estimate that the DIN flux for the entire nonencrusting sponge community is 640 ± 130 micromol m⁻²h⁻₁.
Recent research indicates that coral reef associated benthic algae may control important metabolic processes in reef ecosystems via organic matter release. Yet little information is available about quantity and chemical composition of these algae-derived exudates. Therefore first comprehensive studies on algal organic matter release were conducted at a fringing reef ecosystem in the Northern Red Sea. Dissolved organic carbon (DOC), particulate organic carbon (POC) and nitrogen (PN) release by dominant reef associated benthic algae (Caulerpa serrulata, Peyssonnelia capensis, turf algae assemblages) were quantified during 4 seasonally resolved expeditions. Additionally, 4 seasonal blooming (Ulva lactuca, Enteromorpha flexuosa, Liagora turneri, Hydroclathrus clathratus) and 2 patchy growing algae species (Lobophora variegata, Saragassum dentifolium) were included in these investigations. To complement the dataset organic matter release by Caulerpa was studied under different light conditions, simulating water depths of 1, 5, 10 and 20 m. Environmental parameters (temperature, light availability, inorganic nutrient concentrations) were monitored simultaneously to assess potential effects on algal organic matter release. All 9 investigated genera of benthic algae exuded DOC and POC in amounts of 12.2±2.1 and 4.2±0.3 mg organic C m−² algae surface area h−1, respectively. Resident algae, primarily turf algae assemblages, displayed highest and seasonal blooming algae lowest organic matter release rates. Results therefore indicate that organic matter release rates are rather influenced by functional properties (growth form, life strategy) of algae than by taxonomic affiliation. Quantities of organic matter release showed seasonal and depth-mediated variations and were positively correlated with temperature and light availability within photosynthetically active radiation intensities of 0 to 300 μmol quanta m−2 s−1, suggesting photoinhibition as limiting factor for productivity and subsequent organic matter release. Stable isotope signatures of algae-derived organic carbon were within a common range and likewise subjected to seasonal variations (δ13C summer: −11.2‰±0.2‰; δ13 winter: −16.7‰± 0.4‰). These data provide first comprehensive information about a) the potential contribution of different benthic reef algae to cycles of matter and b) environmental key factors influencing organic matter release by benthic algae in the investigated fringing reef ecosystem.
We show by electrophoresis mobility shift and by DNAase I footprinting assays that the alpha 1 product of the yeast alpha mating-type locus binds to homologous sequences within the control regions of the three known alpha-specific genes. Binding requires both alpha 1 and a second yeast protein(s) (called PRTF) that is present in all three cell types (a, alpha, and a/alpha); neither protein binds alone. Binding and competition experiments using synthetic oligonucleotides indicate that PRTF binds to only part of the homology found at alpha-specific genes and imply that alpha 1 binds to the remainder. Our results suggest that alpha 1 renders gene expression alpha-specific by creating a binding site for PRTF. Similar experiments lead to the idea that PRTF also plays a role in transcription of a-specific genes. Perhaps a-specificity is achieved through the occlusion of the PRTF binding site by alpha 2, the negative regulator encoded by the alpha mating-type locus.