ChapterPDF Available


This chapter provides an introduction to our current understanding of the two most important features of climate change affecting marine sponges—ocean warming and ocean acidification. Of these two stressors, thermal stress associated with ocean warming is likely to have the greatest influence on the sponge assemblages through the induction of diseases and mortality by a decrease in the efficacy of defense mechanisms and development of pathogens. However, there is a considerable variability among species in their responses to increasing temperature, and some species have persisted during episodes of unusually high temperature. Conspicuous sublethal effects have also been described. Thermal stress can limit sponge reproductive capability and dispersal by causing the reabsorption of spermatic cysts and oocytes and by the disruption of the feedback mechanism that prevents the release of asexual propagules when ecological factors are unsuitable for propagule survival. Thermal stress also can affect sponge-feeding behavior by increasing or decreasing filtration rates and by decreasing choanocyte chamber density and size, causing shifts in the microbial communities of the host sponge, and can also increase the production of heat shock proteins, which leads to rapid upregulation of genes involved in cellular damage repair. The effects of ocean acidification on sponges are much less known, but recent studies have demonstrated the resistance of certain species to lowered pH conditions. It seems that this capacity to withstand OA lies in part in the ability of sponges to restructure their host-associated microbiomes mainly by acquiring new microbial components via horizontal transmission. The apparent resilience of some sponge species and the sensitivity of others highlight the need to understand the molecular basis of sponge responses to environmental stressors in order to determine if they will be able to adapt to rapidly changing ocean conditions. Future research focused on transcriptomic and metabolomic responses using genomic approaches will facilitate the assessment of molecular stress responses at different sponge life history stages.
1© Springer International Publishing AG 2017
J.L. Carballo, J.J. Bell (eds.), Climate Change, Ocean Acidication and Sponges,
Chapter 1
Climate Change andSponges: AnIntroduction
JoséLuisCarballo andJamesJ.Bell
Abstract This chapter provides an introduction to our current understanding of the
two most important features of climate change affecting marine sponges—ocean
warming and ocean acidication. Of these two stressors, thermal stress associated
with ocean warming is likely to have the greatest inuence on the sponge assem-
blages through the induction of diseases and mortality by a decrease in the efcacy
of defense mechanisms and development of pathogens. However, there is a consid-
erable variability among species in their responses to increasing temperature, and
some species have persisted during episodes of unusually high temperature.
Conspicuous sublethal effects have also been described. Thermal stress can limit
sponge reproductive capability and dispersal by causing the reabsorption of sper-
matic cysts and oocytes and by the disruption of the feedback mechanism that pre-
vents the release of asexual propagules when ecological factors are unsuitable for
propagule survival. Thermal stress also can affect sponge-feeding behavior by
increasing or decreasing ltration rates and by decreasing choanocyte chamber den-
sity and size, causing shifts in the microbial communities of the host sponge, and
can also increase the production of heat shock proteins, which leads to rapid upregu-
lation of genes involved in cellular damage repair. The effects of ocean acidication
on sponges are much less known, but recent studies have demonstrated the resis-
tance of certain species to lowered pH conditions. It seems that this capacity to
withstand OA lies in part in the ability of sponges to restructure their host- associated
microbiomes mainly by acquiring new microbial components via horizontal trans-
mission. The apparent resilience of some sponge species and the sensitivity of oth-
ers highlight the need to understand the molecular basis of sponge responses to
environmental stressors in order to determine if they will be able to adapt to rapidly
changing ocean conditions. Future research focused on transcriptomic and
J.L. Carballo (*)
Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México
(Unidad Académica Mazatlán), Avenida Joel Montes Camarena s/n,
PO Box 811, Mazatlán C.P.82000, Mexico
J.J. Bell
School of Biological Sciences, Victoria University of Wellington,
PO Box 600, Wellington, New Zealand
metabolomic responses using genomic approaches will facilitate the assessment of
molecular stress responses at different sponge life history stages.
Keywords Sponges • Climate change • Thermal stress • Ocean acidication
1.1 The Two Main Climate Change Factors: Impact ofOW
Shifts in climate regimes are a recurrent feature of the Earth’s history (Zachos etal.
2001), but the peculiarity of modern-day changes is the unprecedented speed at
which they are occurring and the undeniable human inuence (Hansen etal. 2007),
in particular being driven by burning fossil fuels, cement production, and changes
in land use (IPCC 2007). These human activities are rapidly raising the atmospheric
carbon dioxide concentration (CO2) level at a rate that is unprecedented in at least
the last 22,000years (IPCC 2007; Joos and Spahni 2008).
It is predicted that by 2100, the CO2 concentration will be in the range of 541–
970ppm (IPCC 2001), and much of this anthropogenically generated CO2 will be
absorbed by the oceans. The increase in atmospheric carbon dioxide concentration
(CO2) will have two immediate consequences: (1) it will rise Earth’s atmospheric
temperature (global warming, GB) and, particularly, global sea surface tempera-
tures (SSTs) by up to 4°C (IPCC 2007), and (2) it will dissolve in seawater forming
carbonic acid (H2CO3), lowering the pH in a process known as ocean acidication
(OA). In the last 200years, the global ocean pH has dropped by 0.1 pH units (30%
increase in acidity), and it is predicted to drop a further 0.3–0.5units by 2100 (170%
increase in acidity), which is more than 100 times as rapid as at any time over the
past hundreds of the millennia (Meure etal. 2006).
Ocean warming and ocean acidication (pH, pCO2, and calcium carbonate satura-
tion) will impact marine organisms across all levels of biological organization, from
cellular to ecosystem levels. Ocean warming will affect marine benthic ecosystems
through epidemiologic diseases and mass mortalities of invertebrates, in particular
bivalves, corals, and sponges (Harvell etal. 2002; Webster 2007), and also cause coral
bleaching, species invasions, and shifts in species’ latitudinal ranges (Doney et al.
2012). Ocean acidication, in contrast, affects calcifying marine invertebrates most
severely, such as coralline algae (Kuffner etal. 2008), corals (Silverman etal. 2009),
echinoderms, and mollusks (Michaelidis etal. 2005). This is because it decreases the
availability of the carbonate ions required for skeletogenesis; abundanceof particular
group such as pteropod is expected to decline by half during this century due to
increased atmospheric carbon dioxide levels (Orr etal. 2005). OA and particularly
elevated CO2 also affect animals by disrupting the acid-base balance of internal uids,
leading to narcotizing acidosis, and also by triggering physiological mechanisms that
slow or stop metabolism (Knoll etal. 1996). Even more important, reductions in pH
may interfere with ion exchange, depressing metabolism and leading to a narrower
J.L. Carballo and J.J. Bell
window of thermal tolerance (Portner etal. 2005). Organisms that produce CaCO3
skeletons are particularly sensitive to hypercapnia, because carbonate biomineraliza-
tion requires precise control of the acid- base balance (Fabry etal. 2008).
1.2 Marine Sponges: AnIntroduction
Marine sponges are the evolutionary oldest multicellular animals that still exist,
with records from the Precambrian over 700 million years ago (Finks 1970), and a
large and consistent phylogenomic dataset supports sponges as the sister group to
all other animals (Simion etal. 2017).
Their long continued survival since then is closely linked to their simple level of
organization characterized by a lack of organs and true tissues and to the adaptabil-
ity of their body plan. In fact, they have been described as “dynamic multicellular
systems” whose cells have the ability to change into others if they need it, similar to
the stem cells in vertebrates (Bond 1992). This apparently simplistic body structure,
coupled with a unique tolerance to symbiotic microorganisms, gives sponges an
enormous versatility that greatly affects many aspects of their biology and allows
for a great diversity of evolutionary solutions for environmental challenges. In fact,
part of their evolutionary success is ascribed to their intricate association with a
diverse community of microorganisms that occur both intercellularly in the sponge
mesohyl and intracellularly (Thomas etal. 2016) and which can comprise 40–60%
of total tissue volume in some species (Taylor etal. 2007). For this reason, sponges
are described as “holobionts,” that is, a unit comprised of the sponge host and the
consortium of bacteria, archaea, unicellular algae, fungi, and viruses that reside
within it (Webster and Taylor 2012).
Sponges are widely distributed in marine systems and occur mainly in shallow
waters of the continental shelf, but there are species that can be found at 7000m
depth (Hooper and Van Soest 2002). Sponges represent a signicant component of
benthic communities in the oceans with respect to diversity, abundance, and their
potential to inuence benthic or pelagic processes. Thanks to their highly efcient
capability to pump water, over a half liter of water per second per kg dry mass (Weisz
etal. 2008), and the link they provide between nutrient transfer in the open water
column and the benthos, means they are important for benthic-pelagic coupling of
particulate and dissolved carbon (Gili and Coma 1998; Kahn and Leys 2016).
The relationship of sponges with macro- and microbial communities can also
facilitate high levels of benthic primary production and nutrient cycling, including
dissolved carbon (Mohamed etal. 2010; De Goeij et al. 2008), nitrogenous com-
pounds (Corredor et al. 1988; Jiménez and Ribes 2007), silicate (Reincke and
Barthel 1997; Maldonado etal. 2010), and phosphate (Zhang etal. 2015). Because
of this, sponges play a major role in the cycling of dissolved organic matter (DOM)
on coral reefs via the “sponge loop” pathway (de Goeij etal. 2013; Rix etal. 2017).
It has also recently been suggested that calcifying bacterial symbionts of sponges
may have been involved in the early evolution of the skeleton in the Precambrian
1 Climate Change andSponges: AnIntroduction
metazoans and represent a relict mechanism involved in the evolution of skeletons
in lower Metazoa bacteria-mediated skeletonization (Garate etal. 2017).
Sponges are also important habitat builders and can provide hard substrate and
add complexity in otherwise sediment-dominated environments, thereby increasing
abundance and biodiversity of the surrounding area (Dayton etal. 1974; McClintock
etal. 2005). Some species have essential functions in binding unconsolidated sub-
strate such as coral rubble and pebbles into stable surfaces (Wulff 1984). Sponges
are also important bioeroders in coral reefs, coralline bottoms, and oyster beds,
where they are able to excavate tunnels and galleries into calcium carbonate (Rützler
2002; Schönberg 2008; Carballo etal. 2013; Hernández-Ballesteros etal. 2013).
Because of their feeding habits, sponges can accumulate a wide range of pollut-
ants from both the suspension and dissolved phases, and they are considered useful
biomonitoring organisms and can provide convenient tools for characterizing the
state of a marine ecosystem (Carballo etal. 1996; Carballo and Naranjo 2002). They
are capable of accumulating metals (Zahn etal. 1981; Cebrian etal. 2006), organo-
chlorinated compounds (Pérez etal. 2003), radionuclides (Patel etal. 1985), and
combustion-derived PAHs in relation to petrogenic compounds (Batista etal. 2013).
Recently Theonella sp. has been shown to possess a specic and unique bacterial
system for element accumulation and mineralization of both arsenic and barium
(Keren etal. 2017).
1.3 Direct Impacts ofClimate Change onSponges
Unable to escape fromthe alteration of their environment, sponges are particularly
exposed to environmental factors, which control their survival, distribution, and
physiological performance. Thus, the changes associated with climate change will
have diverse consequences on sponge survival and tness. Research into the effects
of climate change on sponges initially focused on thermal sensitivities. Thus, the rst
study that associated a positive thermal anomaly with sponges was that by Vicente
(1989), who suggested that higher water temperature was responsible for the mortal-
ity and extinction of sponges of the genera Spongia and Hippospongia in the
Caribbean. No explanation of the causes of the mortality was given, but a decade
later, in 1999, a massive mortality, also of Spongia, Hippospongia, and Cacospongia,
coincided with a sudden increase in seawater temperature, higher than normal in the
Mediterranean Sea. In this case, it was hypothesized that the cause of that mortality
could be due to an extensive attack by opportunistic protozoans and fungi on the
sponges (Cerrano etal. 2000). Subsequent studies have attributed sponge mortality
to abnormal temperatures as a result of the loss of symbionts and the subsequent
establishment of alien microbial populations, including potential pathogens (Webster
etal. 2008; Cebrián etal. 2011). However, unusually high temperature does affect all
sponge species by the same way. For example, Chondrilla cf. nucula survived during
an episode of unusually high temperature that caused severe coral bleaching in the
Caribbean (Aronson etal. 2002). Furthermore, some encrusting boring sponges tend
J.L. Carballo and J.J. Bell
to spread faster into and over corals, increasing bioerosion and killing corals, during
high temperature events (Rützler 2002). Interestingly, some of these excavating
sponges harbor zooxanthellae in symbioses, which are much less affected by bleach-
ing than corals (Fang etal. 2016).
Unusual increases in temperature not only cause sponge mortality but also affect
physiological performance and reproductive capability and dispersal. Massaro etal.
(2012) showed a signicant reduction in ltration rate and lower choanocyte cham-
ber density and size in Rhopaloeides odorabile at only 2°C higher than the average
ambient seawater temperature. However, this response is not ubiquitous as other
species, such as Halichondria panicea, increased ltration rates at seawater tem-
peratures 5.5 °C above the normal ambient temperature (Riisgard et al. 1993).
Further studies of thermal stress and sponge-feeding ecology are necessary for
determining the mechanisms for this selective behavior. Water temperatures may
have important implications for population reproductive success where oogenesis
and spermatogenesis and larval release are cued by minimum and maximum water
temperatures (Ettinger-Epstein etal. 2007). Thus, thermal stress has been also asso-
ciated with the reabsorption of spermatic cysts and oocytes in the sponge Petrosia
sp. (Asa etal. 2000) and to the disruption of the feedback mechanism that prevents
the release of propagules of C. reniformis when ecological factors do not favor their
survival (Sugni etal. 2014). Surprisingly, Rhopaloeides odorabile larvae are remark-
ably able to withstand seawater temperatures up to 9 °C above normal, despite
adults being susceptible (Webster etal. 2013).
It is important to also mention that unusually low seawater temperatures have
also been associated with the mortality of sponges in temperate latitudes (Pérez
etal. 2006) and to sublethal effects, such as slowing growth and causing contraction
in size of some species (Fowler and Laffoley 1993).
On the other hand, not much is known about the effect of thermal stress on deep
sea sponge populations, despite that mass mortalities of important deep-water popu-
lations of Geodia barrette were associated to an unusual increase of water tempera-
ture in a cold-water coral reef (Norwegian shelf) (Guihen etal. 2012). However,
later studies determined that G. barrette has a high thermal tolerance, and a highly
stable microbiome even at temperatures 5°C above ambient, and that other ecologi-
cal processes such as low oxygen concentrations, elevated nutrients levels and
reduced salinity should be explored to provide insight into the cause:effect path-
ways of G. barrette mortality (Strand etal. 2017). The apparent resilience of some
sponge species and the sensitivity of others highlight the need to understand the
molecular basis of sponge responses to environmental stressors and to understand if
they may be able to adapt to rapidly changing ocean conditions. This was investi-
gated for the rst time in the sponge Suberites domuncula, which expressed a poly-
peptide after heat treatment (Bachinski etal. 1997). Higher-than-normal temperatures
also caused a signicant increase in heat shock protein Hsp70 transcript levels in the
Caribbean sponge Xestospongia muta (López-Legentil etal. 2008) and in Hsp40
and Hsp90 in Rhopaloeides odorabile, indicating the activation of a heat shock
response system. Exposure to high temperatures also produces a rapid downregula-
tion of many genes (actin-related protein, ferritin, calmodulin) and the induction of
1 Climate Change andSponges: AnIntroduction
others involved in signal transduction and in the innate immunity pathways, which
affects expression patterns of genes involved in cellular damage repair, apoptosis,
signaling, and transcription (Pantile and Webster 2011). It is likely that differences
in ecological and physiological features of different sponges, and even their differ-
ent life stages, will reect variations in thermal tolerance and resilience. Haliclona
tubifera subjected to elevated temperature showed activation of various processes
that interact to maintain cellular homeostasis. It seems that this species, which is
normally located in shallow water, is exposed to variable temperatures and has a
more robust response to temperature uctuations compared to sponges found at
deeper depths with colder and more stable temperatures (Guzmán and Conaco
Regarding OA, it has been shown that acidication decreases the diversity, bio-
mass, and trophic complexity of benthic communities (Kroeker etal. 2013). However,
both experimentally (Duckworth etal. 2012) and through eld research of sponges
across natural temperatures and pH ranges, such as those occurring in naturally acidi-
ed areas close to CO2 seeps, have been demonstratedthe resistance of certain sponges
to low-pH conditions (Morrow etal. 2015). It seems that their capacity to withstand
OA lies in their ability to restructure their host-associated microbiomes mainly by
acquiring new microbial components via horizontal transmission (Goodwin et al.
2014). Species with greater microbial diversity may develop functional redundancy
that could enable the holobiont to survive even if particular microbes are lost at low-
pH conditions (Ribes etal. 2016). It has also been suggested that OA may provide a
potential advantage for boring sponges, since OA accelerates bioerosion (Duckworth
and Peterson 2013; Wisshak etal. 2014). Recent research has demonstrated increased
bioerosion rates under experimentally elevated partial pressures of seawater carbon
dioxide (pCO2) with or without increased temperatures, which may lead to net erosion
on coral reefs in the future (Wisshak etal. 2012). However, this may depend on the
ability of sponges to survive and grow in the warmer and more acidic future environ-
ments and, fundamentally, on the energy reserves they have accumulated through the
rest of the year (Fang etal. 2014). It is important to note that there has been relatively
little research investigating about how ocean acidication affects the interaction
between coral and boring sponges, which is important as OA weakens and chemically
dissolves the coral skeletons, making boring easier (Stubler etal. 2014). As seawater
pH decreases, many corals are likely unable to create new layers of calcium carbonate
as efciently resulting in net erosion rates on reefs.
More information of the potential effect of OA on sponges comes from the past.
The overturning of anoxic deep oceans during the Permian-Triassic boundary
occurred about 252 million years ago and introduced high concentrations of carbon
dioxide into surface environments (Knoll etal. 1996), which is thought to be respon-
sible for the extinction of marine organisms that produced calcareous hard parts,
notably reef-building calcareous sponges (Knoll etal. 1996; Pörtner etal. 2004;
Pruss and Bottjer 2005), but also the majority of siliceous sponge species (88–92%),
including all hexactinellids and species with tetraxons (Liu etal. 2008). Low meta-
bolic rate, the absence of a circulatory system, and gas-permeable surfaces may
increase vulnerability in siliceous sponges (Knoll etal. 1996).
J.L. Carballo and J.J. Bell
Most studies concerning the impact of climate change on sponges discuss inde-
pendent effects of warming and ocean acidication, but it is also necessary to
include synergies with other local effects, such as pollution, sedimentation, and
other anthropogenic stressors. Understanding the connection between the different
local effects and climate-related stressors will be also necessary in order to predict
the consequences of future climate change on the survival of sponge populations. It
is also important to predict the biological stress responses of sponges to climate
change and ocean acidication in order to understand how sponges can modify their
gene expression as a potential mechanism for surviving in the future.
Aronson RB, Precht WF, Toscano MA, Koltes KH (2002) The 1998 bleaching event and its after-
math on a coral reef in Belize. Mar Biol 141:435–447
Asa S, Yeemin T, Chaitanawisuti N, Kritsanapuntu A (2000) Sexual reproduction of a marine
sponge, Petrosia sp. from coral communities in the Gulf of Thailand. In: Proceedings 9th inter-
national coral reef symposium, Bali, pp23–27
Bachinski N, Koziol C, Bate R, Labura Z, Schroder HC, Muller WEG (1997) Immediate early
response of the marine sponge Suberites domuncula to heat stress: reduction of trehalose
and glutathione concentrations and glutathione S-transferase activity. J Exp Mar Biol Ecol
Batista D, Tellini K, Nudi AH, Massone TP, Scoeld AL, Wagene A (2013) Marine sponges as bio-
indicators of oil and combustion derived PAH in coastal waters. Mar Environ Res 92:234–243
Bond C (1992) Continuous cell movements rearrange anatomical structures in intact sponges.
JExp Zool 263(3):284–302
Carballo JL, Naranjo S (2002) Environmental assessment of a large industrial marine complex
based on a community of benthic lter feeders. Mar Pollut Bull 44(7):605–610
Carballo JL, Naranjo SA, García-Gómez JC (1996) Use of marine sponges as stress indicators
in marine ecosystems at Algeciras Bay (Southern Iberian peninsula). Mar Ecol Prog Ser
Carballo JL, Bautista E, Nava H, Cruz-Barraza JA, Chávez JA (2013) Boring sponges, an increas-
ing threat for coral reefs affected by bleaching events. Ecol Evol 4:872–886
Cebrian E, Mart R, Agell G, Uriz MJ (2006) Response of the Mediterranean sponge Chondrosia
reniformis Nardo to heavy metal pollution. Environ Pollut 141:452–458
Cebrián E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming
Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS One 6(6):e20211.
Cerrano C, Bavestrello G, Bianchi CN, Cattaneovietti R, Bava S, Morganti C, Morri C, Picco P,
Sara G, Schiaparelli S, Siccardi A, Sponga F (2000) A catastrophic mass-mortality episode of
gorgonians and other organisms in the Ligurian Sea (North-Western Mediterranean), summer
1999. Ecol Lett 3:284–293
Corredor JE, Wilkinson CR, Vicente VP, Morell JM, Otero E (1988) Nitrate release by Caribbean
reef sponges. Limnol Oceanogr 33:114–120
Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic
community at the McMurdo sound, Antarctica. Ecol Monogr 44:105–128
de Goeij JM, Moodley L, Houtekamer M, Carballeira NM, van Duyl FC (2008) Tracing C-13-
enriched dissolved and particulate organic carbon in the bacteria-containing coral reef sponge
Halisarca caerulea: evidence for DOM feeding. Limnol Oceanogr 53:1376–1386
1 Climate Change andSponges: AnIntroduction
de Goeij JM, van Oevelen D, Vermeij M, Osinga R, Middelburg J, de Goeij A etal (2013) Surviving
in a marine desert: the sponge loop retains resources within coral reefs. Science 342:108–110
Doney SC, Ruckelshaus M, Duffy JM, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM,
Hollowed AB, Knowlton N, Polovina P, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate
change impacts on marine ecosystems. Annu Rev Mar Sci 4:11–37
Duckworth AR, Peterson BJ (2013) Effects of seawater temperature and pH on the boring rates of
the sponge Cliona celata in scallop shells. Mar Biol 160(1):27–35
Duckworth AR, West L, Vansach T, Stubler A, Hardt H (2012) Effects of water temperature and
pH on growth and metabolite biosynthesis of coral reef sponges. Mar Ecol Prog Ser 462:67–77
Ettinger-Epstein P, Whalan S, Battershill CN, de Nys R (2007) Temperature cues gametogenesis
and larval release in a tropical sponge. Mar Biol 153:171–178
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidication on marine fauna and
ecosystem process. ICES JMar Sci 65:414–432
Fang JKH, Schönberg CHL, Mello-Athayde MA, Hoegh-Guldberg O, Dove S (2014) Effects of
ocean warming and acidication on the energy budget of an excavating sponge. Glob Change
Biol 20:1043–1054
Fang JKH, Schönberg CHL, Hoegh-Guldberg O, Dove S (2016) Day–night ecophysiology of the
photosymbiotic bioeroding sponge Cliona orientalis Thiele 1900. Mar Biol 163:1–12
Finks RM (1970) The evolution and the ecological history of sponges during Paleozoic times.
Symp Zool Soc Lond 25:3–22
Fowler S, Laffoley D (1993) Stability in Mediterranean-Atlantic sessile epifaunal communities at
the northern limits of their range. JExp Mar Biol Ecol 172:109–127
Garate L, Sureda J, Agell G, Uriz MJ (2017) Endosymbiotic calcifying bacteria across sponge
species and oceans. Sci Rep. 7:43674
Gili JM, Coma R (1998) Benthic suspension feeders: their paramount role in littoral marine food
webs. Trends Ecol Evol 13:316–321
Goodwin C, Metalpa RR, Bernard P, Hall-Spencer JM (2014) Effects of ocean acidication on
sponge communities. Mar Ecol 35:41–49
Guihen D, White M, Lundalv T (2012) Temperature shocks and ecological implications at a cold-
water coral reef. Mar Biodiversity 5:e68. doi:10.1017/S1755267212000413
Guzmán C, Conaco C (2016) Gene expression dynamics accompanying the sponge thermal stress
response. PLoS One 11(10):e0165368. doi:10.1371/journal.pone.0165368
Hansen J, Sato M, Ruedy R, Kharecha P, Lacis A, Miller R, Nazarenko L, Lo K, Schmidt GA,
Russell G etal (2007) Dangerous human-made interference with climate: a GISS model study.
Atmos Chem Phys 7:2287–2312
Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate
warming and disease risks for terrestrial and marine biota. Science 296:2158–2162
Hernández-Ballesteros LM, Elizalde-Rendón EM, Carballo JL, Carricart-Ganivet JP (2013)
Sponge bioerosion on reef-building corals: dependent on the environment or on skeletal den-
sity? JExp Mar Biol Ecol 441:23–27
Hooper RWM, Van Soest RWM (2002) Systema porifera. A guide to the classication of sponges,
vol 1. Kluwer Academic/Plenum Publishers, NewYork
IPCC (2001) In: Houghton JT, Ding Y, Griggs DJ, Noguer M, van der Linden PJ, Dai X, Maskell
K, John-son CA (eds) Report: climate change: the scientic basis. Cambridge University Press,
IPCC (2007) In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M,
Miller HL (eds) Climate change 2007: the physical science basis. Contribution of working
group I to the fourth assessment report of the intergovernmental panel on climate change.
Cambridge University Press, Cambridge, p996
Jiménez E, Ribes M (2007) Sponges as a source of dissolved inorganic nitrogen: nitrication
media ted by temperate sponge. Limnol Oceanogr 52(3):948–958
Joos F, Spahni R (2008) Rates of change in natural and anthropogenic radiative forcing over the
past 20,000 years. Proc Natl Acad Sci U S A 105:1425–1430
J.L. Carballo and J.J. Bell
Kahn AS, Leys SP (2016) The role of cell replacement in benthic–pelagic coupling by suspension
feeders. R Soc Open Sci 3:160484. doi:10.1098/rsos.160484
Keren R, Mayzel M, Lavy A, Polishchuk I, Levy D, Fakra SC, Pokroy B, Ilan M (2017) Sponge-
associated bacteria mineralize arsenic and barium on intracellular vesicles. Nat Commun
8:14393. doi:10.1038/ncomms14393
Knoll AH, Bambach RK, Caneld DE, Grotzinger JP (1996) Comparative earth history and Late
Permain mass extinction. Science 273:452–457
Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, Singh GS, Duarte CM, Gattuso JP
(2013) Impacts of ocean acidication on marine organisms: quantifying sensitivities and inter-
action with warming. Glob Change Biol 19:1884–1896
Kuffner IB, Andersson AJ, Jokiel PL, Rodgers KS, Mackenzie FT (2008) Decreased abundance of
crustose coralline algae due to ocean acidication. Nat Geosci 1:114–117
Liu G, Feng Q, Gu S (2008) Extinction pattern and process of siliceous sponge spicules in deep-
water during the latest Permian in South China. Sci China Ser D Earth Sci 51:1623–1632
López-Legentil S, Song B, McMurray SE, Pawlik JR (2008) Bleaching and stress in coral reef
ecosystems: hsp70 expression by the giant barrel sponge Xestospongia muta. Mol Ecol
Maldonado M, Riesgo A, Bucci A, Rützler K (2010) Revisiting silicon budgets at a tropical con-
tinental shelf: silica standing stocks in sponges surpass those in diatoms. Limnol Oceanogr
Massaro AJ, Weisz JB, Hill MS, Webster NS (2012) Behavioral and morphological changes caused
by thermal stress in the great barrier reef sponge Rhopaloeides odorabile. JExp Mar Biol Ecol
McClintock JB, Amsler CD, Baker BJ, van Soest RWM (2005) Ecology of Antarctic marine
sponges: an overview. Integr Comp Biol 45(2):359–368
Meure CM, Etheridge D, Trudinger C, Steele P, Langenfelds R, van Ommen T, Smith A, Elkins
J(2006) Law dome CO2, CH4 and N2O ice core records extended to 2000 years BP.Geophys.
Res Lett 33:L14810
Michaelidis B, Ouzounis C, Paleras A, Pörtner HO (2005) Effects of long-term moderate hyper-
capnia on acid–base balance and growth rate in marine mussels Mytilus galloprovincialis. Mar
Ecol Prog Ser 293:109–118
Mohamed NM, Saito K, Tal Y, Hill RT (2010) Diversity of aerobic and anaerobic ammonia-
oxidizing bacteria in marine sponges. ISME J4:38–48
Morrow KM, Bourne DG, Humphrey C, Botte ES, Laffy P, Zaneveld J, Uthicke S, Fabricius KE,
Webster NS (2015) Natural volcanic CO2 seeps reveal future trajectories for host–microbial
associations in corals and sponges. ISME J9:894–908
Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida
A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear M, Monfray P, Mouchet A, Najjar
RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ,
Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidication over the twenty-rst
century and its impact on calcifying organisms. Nature 437:681–686
Pantile R, Webster NS (2011) Strict thermal threshold identied by quantitative PCR in the sponge
Rhopaloeides odorabile. Mar Ecol Prog Ser 431:97–105
Patel B, Patel S, Balani MC (1985) Can a sponge fractionate isotopes? Proc R Soc Lond. B Biol
Sci 224(1234):23–41
Pérez T, Wafo E, Fourt M, Vacelet J(2003) Marine sponges as biomonitor of polychlorobiphenyls
contamination: concentration and fate of 24 congeners. Environ Sci Technol 37(10):2152–2158
Pérez T, Perrin B, Carteron S, Vacelet J, Boury-Esnault N (2006) Celtodoryx morbihanensis gen.
nov. sp. nov., a new sponge species (Poecilosclerida, Demospongiae) invading the Gulf of
Morbihan (NE Atlantic-France). Cah Biol Mar 47:205–214
Pörtner HO, Langenbuch M, Reipschläger A (2004) Biological impact of elevated ocean CO2 con-
centrations: lessons from animal physiology and earth history. JOceanogr 60:705–718
Portner HO, Langenbuch M, Michaelidis B (2005) Synergistic effects of temperature extremes,
hypoxia, and increases in CO2 on marine animals: from earth history to global change.
JGeophys Res Oceans 110:15
1 Climate Change andSponges: AnIntroduction
Pruss SB, Bottjer DJ (2005) The reorganization of reef communities following the end-Permian
mass extinction. C R Palevol 4:553–568
Reincke T, Barthel D (1997) Silica uptake kinetics of Halichondria panicea in Kiel bight. Mar
Biol 129:591
Ribes M, Calvo E, Movilla J, Logares R, Coma R, Pelejero C (2016) Restructuring of the sponge
microbiome favors tolerance to ocean acidication. Environ Microbiol Rep 8(4):536–544
Riisgard HU, Thomassen S, Jakobsen H, Weeks JM, Larsen PS (1993) Suspension feeding in
marine sponges Halichondria panicea and Haliclona urceolus: effects of temperature on ltra-
tion rate and energy cost of pumping. Mar Ecol Progr Ser 96:177–188
Rix L, de Goeij JM, van Oevelen D, Struck U, Al-Horani FA, Wild C, Naumann MS (2017)
Differential recycling of coral and algal dissolved organic matter via the sponge loop. Funct
Ecol 31:778–789
Rützler K (2002) Impact of crustose clionid sponges on Caribbean reef corals. Acta Geol Hisp
Schönberg CHL (2008) A history of sponge erosion: from past myths and hypotheses to recent
approaches. In: Wisshak M, Tapanila L (eds) Erlangen earth conference series. Current devel-
opments in bioerosion. Springer, Berlin, pp165–202
Silverman J, Lazar B, Cao L, Caldeira K, Erez L (2009) Coral reefs may start dissolving when
atmospheric CO2 doubles. Geophys Res Lett 36:L05606. doi:10.1029/2008GL036282. 200
Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, Roure B, Satoh N, Quéinnec
E etal (2017) A large and consistent phylogenomic dataset supports sponges as the sister group
to all other animals. Curr Biol 27(7):958–967. doi:10.1016/j.cub.2017.02.031
Strand R, Whalan S, Webster NS, Kutti T, Fang JKH, Luter HM, Bannister RJ (2017) The
response of a boreal deep-sea sponge holobiont to acute thermal stress. Sci Rep 7. doi:10.1038/
Stubler AD, Furman BT, Peterson BJ (2014) Effects of pCO2 on the interaction between an excavat-
ing sponge Cliona varians, and a hermatypic coral, Porites furcata. Mar Biol 161:1851–1859
Sugni M, Fassini D, Barbaglio A, Biressi A, Di Benedetto C, Tricarico S, Bonasoro F, Wilkie
I, Candia Carneval MD (2014) Comparing dynamic connective tissue in echinoderms and
sponges: morphological and mechanical aspects and environmental sensitivity. Mar Environ
Res 93:123–132
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution,
ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347
Thomas T, Moitinho-Silva L, Lurgi M, Björk JR, Easson C, Astudillo-García C, Olson JB,
Erwin PM, López-Legentil S, Luter H, Chaves-Fonnegra A, Costa R, Schupp PJ, Steindler L,
Erpenbeck D, Gilbert J, Knight R, Ackermann G, Victor Lopez J, Taylor MW, Thacker RW,
Montoya JM, Hentschel U, Webster NS (2016) Diversity, structure and convergent evolution of
the global sponge microbiome. Nat Commun 7:11870
Vicente VP (1989) Regional commercial sponge extinctions in the West Indies: are recent climatic
changes responsible. Mar Ecol 10(2):179–191
Webster N (2007) Sponge disease: a global threat? Environ Microbiol 9(6):1363–1375
Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other
relationships. Environ Microbiol 14:335–346
Webster NS, Cobb RE, Negri AP (2008) Temperature thresholds for bacterial symbiosis with a
sponge. ISME J2:830–842
Webster N, Pantile R, Botte E, Abdo D, Andreakis N, Whalan S (2013) A complex life cycle in a
warming planet: gene expression in thermally stressed sponges. Mol Ecol. 22(7):1854–1868
Weisz JB, Lindquist N, Martens CS (2008) Do associated microbial abundances impact marine
demosponge pumping rates and tissue densities? Oecologia 155:367–376
Wisshak M, Schönberg CHL, Form AU, Freiwald A (2012) Ocean acidication accelerates reef
bioerosion. PLoS One 7:e45124
Wisshak M, Schonberg CHL, Form A, Freiwald A (2014) Sponge bioerosion accelerated by ocean
acidication across species and latitudes? Helgol Mar Res 68:253–262
J.L. Carballo and J.J. Bell
Wulff JL (1984) Sponge-mediated coral reef growth and rejuvenation. Coral Reefs 3:157–163
Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in
global climate 65Ma to present. Science 292:686–693
Zahn RK, Zahn G, Muller WEG, Kurelec B, Rijavec M, Batel R, Given R (1981) Assessing con-
sequences of marine pollution by hydrocarbons using sponges as model organisms. Sci Total
Environ 20(2):147–169
Zhang F, Blasiak LC, Karolin JO, Powell RJ, Geddes CD, Hill RT (2015) Phosphorus sequestra-
tion in the form of polyphosphate by microbial symbionts in marine sponges. Proc Natl Acad
Sci U S A 112:4381–4386
1 Climate Change andSponges: AnIntroduction
... Sponges are filter-feeding basal organisms with a long evolutionary history (convincingly documented from lower Cambrian to recent) and are regarded by many scientists as one of the most primitive living animals. These sessile benthic organisms with rapid larval settlement are recognized as dynamic multicellular systems capable of living in various types of aquatic environments, usually comprising a significant portion of benthic communities (Bond, 1992;Carballo and Bell, 2017). They can help build hard substrates for benthic communities and can positively influence the levels of primary production and nutrition cycles (Jiménez and Ribes, 2007;De Goeij et al., 2008;Mohamed et al., 2010;Carballo and Bell, 2017). ...
... These sessile benthic organisms with rapid larval settlement are recognized as dynamic multicellular systems capable of living in various types of aquatic environments, usually comprising a significant portion of benthic communities (Bond, 1992;Carballo and Bell, 2017). They can help build hard substrates for benthic communities and can positively influence the levels of primary production and nutrition cycles (Jiménez and Ribes, 2007;De Goeij et al., 2008;Mohamed et al., 2010;Carballo and Bell, 2017). ...
The sponges may be the oldest group of Metazoa, with a long and successful evolutionary history. Despite their intermittent fossil record quality, the group has been considered reliable for paleoecological and paleobiogeographic analyses because they have inhabited various types of aquatic environments, forming a significant part of benthic communities. We have presented a detailed description of a new species from the genus Teganiella , Teganiella finksi new species, which expands the chronologic range and classifies the genus as endemic to the paleoequatorial regions of Laurentia associated with arid climate conditions linked to hypersaline periods. Combining the paleoecological and paleoenvironmental features of the Teganiella species, our findings also suggest a trend toward more closed-inlet conditions, which may be related to competition and/or specific habitat supplies, for example, heavy metals such as vanadium, zinc, and molybdenum. UUID:
... Sponges are characterized by a simple level of organization, lack of organs, nervous system, and true tissues, and are efficient filter-feeding (Reid, 2003). Despite their apparent simplistic body structure sponges have a long-continued survival and a high diversity that still exist (Carballo and Bell, 2017). ...
Archaeocyaths, articulated reticulosans, protospongiid sponge spicules, fragments of chancelloriid scleritomes and isolated sclerites are typical components of the lower-middle Cambrian Sonora biota of Mexico. This report briefly introduces the Cambrian sponges and chancelloriid fossils of the Sonoran platform described and illustrated to date. Early Cambrian (Series 2, stages 3 and 4) sponge spicules, Kiwetinokia sp. and extinct sponge-like archaeocyaths occur in the Puerto Blanco Formation, at the Cerro Clemente and Cerro Rajón in the Caborca region, northwest Sonora. Besides, a variety of chancelloriid sclerites belonging to Chancelloria, Allonia, and Archiasterella have been described in that region. Also, Chancelloria sclerites have been documented in the Arrojos Formation of the Caborca region. A fauna of hexactinellid sponges and chancelloriids was recorded from the middle Cambrian (Wuliuan Stage, Miaolingian Series) strata from the Arivechi section, in the eastern part, and San José de Gracia and El Sahural sections in the central Sonora. The middle Cambrian El Mogallón Formation in the Arivechi area yield assemblages of reticulosan thin-wall sponges, isolated protospongiid spicules and chancelloriid sclerite morphotypes. Fragments of articulated scleritomes of Chancelloria eros were reported for the first time for the Cambrian of Mexico, and sclerites of Allonia and Archiasterella in the Cerro El Sahuaral near San José de Gracia. Protospongiid spicules and isolated sclerites of chancelloriids were determined in the Cerro El Chihuarruita section at the San José de Gracia area. The mid-Cambrian Sonoran faunas have been compared with the Burgess Shale biota in Canada, and those of the Utah formations, in the USA localized around the Laurentia. Nevertheless, as the chancelloriid fauna is cosmopolitan, some of these genera are also present in other palaeocontinent including Siberia, China, and Australia. Sponges and chancelloriids are an important biotic component of the Sonoran communities. Their discovery constitutes a valuable tool for the reconstruction of the faunas, their paleoecology and paleoenvironments. These findings expand the paleogeographical distribution of these faunas during the Cambrian in the warm platform of Sonora.
... Thermal stress in particular can decrease efficacy of defense mechanisms, leading to increased mortality due to pathogens and diseases. In addition, ocean warming can lead to species invasion, shifts in species' latitudinal ranges, and bleaching (Carballo and Bell, 2017). ...
Full-text available
Interest in bioactive pigments stems from their ecological role in adaptation, as well as their applications in various consumer products. The production of these bioactive pigments can be from a variety of biological sources, including simple microorganisms that may or may not be associated with a host. This study is particularly interested in the marine sponges, which have been known to harbor microorganisms that produce secondary metabolites like bioactive pigments. In this study, marine sponge tissue samples were collected from Puhi Bay off the Eastern shore of Hilo, Hawai‘i and subsequently were identified as Petrosia sp. with red pigmentation. Using surface sterilization and aseptic plating of sponge tissue samples, sponge-associated microorganisms were isolated. One isolate (PPB1) produced a colony with red pigmentation like that of Petrosia sp., suggesting an integral relationship between this particular isolate and the sponge of interest. 16S characterization and sequencing of PPB1 revealed that it belonged to the Pseudoalteromonas genus. Using various biological assays, both antimicrobial and antioxidant bioactivity was shown in Pseudoalteromonas sp. PPB1 crude extract. To further investigate the genetics of pigment production, a draft genome of PPB1 was sequenced, assembled, and annotated. This revealed a prodiginine biosynthetic pathway and the first cited-incidence of a prodiginine-producing Pseudoalteromonas species isolated from a marine sponge host. Further understanding into the bioactivity and biosynthesis of secondary metabolites like pigmented prodiginine may uncover the complex ecological interactions between host sponge and microorganism.
... Ocean warming is thought to cause increased thermal stress on sponge assemblages. This stress could cause disease and mortality owing to a decrease in the efficacy of defence mechanisms, and via the development of pathogens 32 . There are currently no commercial bottom fisheries within the South Orkney area, however, demersal fishing is occurring in other areas with similar habitats and ecology. ...
Full-text available
Antarctic sea-floor communities are unique, and more closely resemble those of the Palaeozoic than equivalent contemporary habitats. However, comparatively little is known about the processes that structure these communities or how they might respond to anthropogenic change. In order to investigate likely consequences of a decline or removal of key taxa on community dynamics we use Bayesian network inference to reconstruct ecological networks and infer changes of taxon removal. Here we show that sponges have the greatest influence on the dynamics of the Antarctic benthos. When we removed sponges from the network, the abundances of all major taxa reduced by a mean of 42%, significantly more than changes of substrate. To our knowledge, this study is the first to demonstrate the cascade effects of removing key ecosystem structuring organisms from statistical analyses of Antarctica data and demonstrates the importance of considering the community dynamics when planning ecosystem management.
... cope with increases in temperature are limited in scope and number (Bell et al., 2015;Carballo & Bell, 2017). ...
Full-text available
Although the cellular and molecular responses to exposure to relatively high temperatures (acute thermal stress or heat shock) have been studied previously, only sparse empirical evidence of how it affects cold-water species is available. As climate change becomes more pronounced in areas such as the Western Antarctic Peninsula, both long-term and occasional acute temperature rises will impact species found there, and it has become crucial to understand the capacity of these species to respond to such thermal stress. Here, we use the Antarctic sponge Isodictya sp. to investigate how sessile organisms (particularly Porifera) can adjust to acute short-term heat stress, by exposing this species to 3 and 5 °C for 4 h, corresponding to predicted temperatures under high-end 2080 IPCC-SRES scenarios. Assembling a de novo reference transcriptome (90,188 contigs, >93.7% metazoan BUSCO genes) we have begun to discern the molecular response employed by Isodictya to adjust to heat exposure. Our initial analyses suggest that TGF-β, ubiquitin and hedgehog cascades are involved, alongside other genes. However, the degree and type of response changed little from 3 to 5 °C in the time frame examined, suggesting that even moderate rises in temperature could cause stress at the limits of this organism’s capacity. Given the importance of sponges to Antarctic ecosystems, our findings are vital for discerning the consequences of short-term increases in Antarctic ocean temperature on these and other species.
Full-text available
Effects of elevated seawater temperatures on deep-water benthos has been poorly studied, despite reports of increased seawater temperature (up to 4 °C over 24 hrs) coinciding with mass mortality events of the sponge Geodia barretti at Tisler Reef, Norway. While the mechanisms driving these mortality events are unclear, manipulative laboratory experiments were conducted to quantify the effects of elevated temperature (up to 5 °C, above ambient levels) on the ecophysiology (respiration rate, nutrient uptake, cellular integrity and sponge microbiome) of G. barretti. No visible signs of stress (tissue necrosis or discolouration) were evident across experimental treatments; however, significant interactive effects of time and treatment on respiration, nutrient production and cellular stress were detected. Respiration rates and nitrogen effluxes doubled in responses to elevated temperatures (11 °C & 12 °C) compared to control temperatures (7 °C). Cellular stress, as measured through lysosomal destabilisation, was 2–5 times higher at elevated temperatures than for control temperatures. However, the microbiome of G. barretti remained stable throughout the experiment, irrespective of temperature treatment. Mortality was not evident and respiration rates returned to pre-experimental levels during recovery. These results suggest other environmental processes, either alone or in combination with elevated temperature, contributed to the mortality of G. barretti at Tisler reef.
Full-text available
From an evolutionary point of view, sponges are ideal targets to study marine symbioses as they are the most ancient living metazoans and harbour highly diverse microbial communities. A recently discovered association between the sponge Hemimycale columella and an intracellular bacterium that generates large amounts of calcite spherules has prompted speculation on the possible role of intracellular bacteria in the evolution of the skeleton in early animals. To gain insight into this purportedly ancestral symbiosis, we investigated the presence of symbiotic bacteria in Mediterranean and Caribbean sponges. We found four new calcibacteria OTUs belonging to the SAR116 in two orders (Poecilosclerida and Clionaida) and three families of Demospongiae, two additional OTUs in cnidarians and one more in seawater (at 98.5% similarity). Using a calcibacteria targeted probe and CARD-FISH, we also found calcibacteria in Spirophorida and Suberitida and proved that the calcifying bacteria accumulated at the sponge periphery, forming a skeletal cortex, analogous to that of siliceous microscleres in other demosponges. Bacteria-mediated skeletonization is spread in a range of phylogenetically distant species and thus the purported implication of bacteria in skeleton formation and evolution of early animals gains relevance.
Full-text available
Arsenic and barium are ubiquitous environmental toxins that accumulate in higher trophic-level organisms. Whereas metazoans have detoxifying organs to cope with toxic metals, sponges lack organs but harbour a symbiotic microbiome performing various functions. Here we examine the potential roles of microorganisms in arsenic and barium cycles in the sponge Theonella swinhoei, known to accumulate high levels of these metals. We show that a single sponge symbiotic bacterium, Entotheonella sp., constitutes the arsenic-and barium-accumulating entity within the host. These bacteria mineralize both arsenic and barium on intracellular vesicles. Our results indicate that Entotheonella sp. may act as a detoxifying organ for its host.
Full-text available
Benthic-pelagic coupling through suspension feeders and their detrital pathways is integral to carbon transport in oceans. In food-poor ecosystems however, a novel mechanism of carbon recycling has been proposed that involves direct uptake of dissolved carbon by suspension feeders followed by shedding of cells as particulate carbon. We studied cell replacement rates in a range of cold-water sponge species to determine how universal this mechanism might be. We show that cell replacement rates of feeding epithelia in explants vary from 30 hours up to 7 days, and change during different seasons and life-history stages. We also found that feeding epithelia are not replaced through direct replication but instead arise from a population of stem cells that differentiate and integrate into epithelial tissues. Our results reveal a surprising amount of complexity in the control of cell processes in sponges, with cell turnover depending on environmental conditions and using stem cells as rate-limitingmechanisms. Our results also suggest that for species in cold water with high particulate organic matter, cell turnover is not the mechanism delivering carbon flux to surrounding communities.
Full-text available
Marine sponges are important members of coral reef ecosystems. Thus, their responses to changes in ocean chemistry and environmental conditions, particularly to higher seawater temperatures, will have potential impacts on the future of these reefs. To better understand the sponge thermal stress response, we investigated gene expression dynamics in the shallow water sponge, Haliclona tubifera (order Haplosclerida, class Demospongiae), subjected to elevated temperature. Using high-throughput transcriptome sequencing, we show that these conditions result in the activation of various processes that interact to maintain cellular homeostasis. Short-term thermal stress resulted in the induction of heat shock proteins, antioxidants, and genes involved in signal transduction and innate immunity pathways. Prolonged exposure to thermal stress affected the expression of genes involved in cellular damage repair, apoptosis, signaling and transcription. Interestingly, exposure to sublethal temperatures may improve the ability of the sponge to mitigate cellular damage under more extreme stress conditions. These insights into the potential mechanisms of adaptation and resilience of sponges contribute to a better understanding of sponge conservation status and the prediction of ecosystem trajectories under future climate conditions.
Full-text available
Summary Corals and macroalgae release large quantities of dissolved organic matter (DOM), one of the largest sources of organic matter produced on coral reefs. By rapidly taking up DOM and transforming it into particulate detritus, coral reef sponges are proposed to play a key role in transferring the energy and nutrients in DOM to higher trophic levels via the recently discovered sponge loop. DOM released by corals and algae differs in quality and composition, but the influence of these different DOM sources on recycling by the sponge loop has not been investigated. Here, we used stable isotope pulse-chase experiments to compare the processing of naturally sourced coral- and algal-derived DOM by three Red Sea coral reef sponge species: Chondrilla sacciformis, Hemimycale arabica and Mycale fistulifera. Incubation experiments were conducted to trace 13C- and 15N-enriched coral- and algal-derived DOM into the sponge tissue and detritus. Incorporation of 13C into specific phospholipid-derived fatty acids (PLFAs) was used to differentiate DOM assimilation within the sponge holobiont (i.e. the sponge host vs. its associated bacteria). All sponges assimilated both coral- and algal-derived DOM, but incorporation rates were significantly higher for algal-derived DOM. The two DOM sources were also processed differently by the sponge holobiont. Algal-derived DOM was incorporated into bacteria-specific PLFAs at a higher rate while coral-derived DOM was more readily incorporated into sponge-specific PLFAs. A substantial fraction of the dissolved organic carbon (C) and nitrogen (N) assimilated by the sponges was subsequently converted into and released as particulate detritus (15–24% C and 27–49% N). However, algal-derived DOM was released as detritus at a higher rate. The higher uptake and transformation rates of algal- compared with coral-derived DOM suggest that reef community phase shifts from coral to algal dominance may stimulate DOM cycling through the sponge loop with potential consequences for coral reef biogeochemical cycles and food webs.
Full-text available
Sponges (phylum Porifera) are early-diverging metazoa renowned for establishing complex microbial symbioses. Here we present a global Porifera microbiome survey, set out to establish the ecological and evolutionary drivers of these host-microbe interactions. We show that sponges are a reservoir of exceptional microbial diversity and major contributors to the total microbial diversity of the world's oceans. Little commonality in species composition or structure is evident across the phylum, although symbiont communities are characterized by specialists and generalists rather than opportunists. Core sponge microbiomes are stable and characterized by generalist symbionts exhibiting amensal and/or commensal interactions. Symbionts that are phylogenetically unique to sponges do not disproportionally contribute to the core microbiome, and host phylogeny impacts complexity rather than composition of the symbiont community. Our findings support a model of independent assembly and evolution in symbiont communities across the entire host phylum, with convergent forces resulting in analogous community organization and interactions.
Full-text available
Ocean acidification is increasing and affects many marine organisms. However, certain sponge species can withstand low-pH conditions. This may be related to their complex association with microbes. We hypothesized that species with greater microbial diversity may develop functional redundancy that could enable the holobiont to survive even if particular microbes are lost at low-pH conditions. We evaluated the effects of acidification on the growth and associated microbes of three ubiquitous Mediterranean sponges by exposing them to the present pH level and that predicted for the year 2100. We found marked differences among the species in the acquisition of new microbes, being high in Dysidea avara, moderate in Agelas oroides and null in Chondrosia reniformis; however, we did not observe variation in the overall microbiome abundance, richness or diversity. The relative abilities to alter the microbiomes contributes to survivorship in an OA scenario as demonstrated by lowered pH severely affecting the growth of C. reniformis, halving that of A. oroides, and unaffecting D. avara. Our results indicate that functional stability of the sponge holobiont to withstand future OA is species-specific and is linked to the species' ability to use horizontal transmission to modify the associated microbiome to adapt to environmental change.
Resolving the early diversification of animal lineages has proven difficult, even using genome-scale datasets. Several phylogenomic studies have supported the classical scenario in which sponges (Porifera) are the sister group to all other animals (“Porifera-sister” hypothesis), consistent with a single origin of the gut, nerve cells, and muscle cells in the stem lineage of eumetazoans (bilaterians + ctenophores + cnidarians). In contrast, several other studies have recovered an alternative topology in which ctenophores are the sister group to all other animals (including sponges). The “Ctenophora-sister” hypothesis implies that eumetazoan-specific traits, such as neurons and muscle cells, either evolved once along the metazoan stem lineage and were then lost in sponges and placozoans or evolved at least twice independently in Ctenophora and in Cnidaria + Bilateria. Here, we report on our reconstruction of deep metazoan relationships using a 1,719-gene dataset with dense taxonomic sampling of non-bilaterian animals that was assembled using a semi-automated procedure, designed to reduce known error sources. Our dataset outperforms previous metazoan gene superalignments in terms of data quality and quantity. Analyses with a best-fitting site-heterogeneous evolutionary model provide strong statistical support for placing sponges as the sister-group to all other metazoans, with ctenophores emerging as the second-earliest branching animal lineage. Only those methodological settings that exacerbated long-branch attraction artifacts yielded Ctenophora-sister. These results show that methodological issues must be carefully addressed to tackle difficult phylogenetic questions and pave the road to a better understanding of how fundamental features of animal body plans have emerged.