Guibert, Isis

Global Change Biology

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Glob Change Biol. 2024;30:e17150.	 	 	 | 1 of 3https://doi.org/10.1111/gcb.17150wileyonlinelibrary.com/journal/gcbReceived:	27	November	2023  | Revised:	18	December	2023  | Accepted:	29	December	2023DOI:	10.1111/gcb.17150		I N V I T E D  C O M M E N T A R YAssisted evolution of algal symbionts to enhance coral reef bleaching tolerance: A success storyIsis GuibertSchool	of	Biological	Sciences,	The	University	of	Hong	Kong,	Hong	Kong	SAR,	ChinaCorrespondenceIsis	Guibert,	School	of	Biological	Sciences,	The	University	of	Hong	Kong,	Hong	Kong	SAR,	China.Email: iguibert@hku.hkKEYWORDScoral, experimental evolution, reef restoration, Symbiodinicaeae, thermotoleranceCoral	reefs	host	a	diversity	of	organisms,	providing	ecosystem	goods	and	 services	 for	more	 than	500 million	people	worldwide	 (Hoegh-	Guldberg	 et	 al.,	 2019). Unprecedented threats, such as increasing human population, fishing pressure, and ocean acidification are de-creasing the ability of coral ecosystems to provide these valuable goods and services. Perhaps the most alarming of these threats is anthropogenic global warming, which is leading to severe effects on coral, disrupting the association between coral host and symbiont microalgae and resulting in bleaching of coral and potential coral death	 (Hughes	et	 al.,	 2018). The survival of corals hinges on their ability to maintain symbiotic associations with microalgae from the Symbiodiniaceae family, as these microalgae provide vital carbon and	nitrogen	to	their	hosts	 (Quigley	et	al.,	2023). Symbiodiniaceae possess physiological properties that can provide protection to their hosts during stress events, such as increased tolerance to high temperatures. However, even these resilient Symbiodiniaceae can-not withstand the onslaught of intense marine heatwaves, which have	 been	 linked	 to	 reef	 decline	 in	 the	 last	 few	decades	 (Hughes	et al., 2018).	With	an	estimated	loss	of	90%	of	the	world's	coral	reefs	predicted	by	2050	(Hughes	et	al.,	2018), it is imperative that we ex-plore solutions to safeguard these fragile coral ecosystems.In	 anticipation	 of	 the	 severe	 ocean	 warming	 and	 acidification	expected	for	the	near	future	(IPCC,	2022), advanced techniques to maintain	 coral	 reefs	 are	 actively	 being	 explored.	 Human-	assisted	evolution is a new area of research aiming to transplant manipu-lated coral into the natural environment to establish resilient coral reefs	 (van	 Oppen	 et	 al.,	 2015).	 The	 host-	associated	 microbiome	has been revealed as essential for the adaptation of corals to their environment, making it a significant consideration in conservation biology.	 Microbiome-	based	 interventions	 have	 primarily	 focused	on	 the	 use	 of	 probiotics	 to	 enhance	 coral	 host	 resilience	 (Peixoto	et al., 2021). Similarly, the manipulation of genetic variants of algal symbionts is promising due to their short generation time com-pared to their coral host, enabling them to evolve more rapidly (Chakravarti,	2019). The ability to culture algal symbionts and pre-cisely control their environmental conditions offers potential for rapid thermal adaptation. However, there are practical limitations regarding the number of species that can be manipulated and the cost	associated	with	such	approaches	(Anthony,	2016).	Additionally,	the	 risk	 of	 biodiversity	 loss	 is	 non-	negligible	 due	 to	 the	 potential	spread	 of	 a	 few	 resistant	 species	 (Anthony,	 2016). Nevertheless, given the high value of coral reefs and the current trend of coral species losing the battle against global warming, preserving a few keystone species will sustain some ecosystem goods and services and prove more favorable than facing a total decline of coral reefs.Among	the	different	genera	of	Symbiodiniaceae,	Durusdinium confers	 higher	 thermotolerances	 in	 Indo-	Pacific	 scleractinian	corals compared to the most widespread genus, Cladocopium (LaJeunesse,	2005;	Palacio-	Castro	et	al.,	2023). However, it is im-portant to note that Durusdinium	 sp.	 confers	 certain	 trade-	offs,	such as inhibiting coral growth and translocation to the host. This makes Cladocopium	a	more	favorable	candidate	for	producing	heat-	evolved Symbiodiniaceae. Recent research has demonstrated the positive	impact	of	heat-	evolved	strains	of	Cladocopium proliferum (specifically	 SS1,	 SS7,	 and	 SS8)	 when	 inoculated	 to	Acropora te-nuis larvae, resulting in enhanced thermal tolerance compared This is an open access article under the terms of the Creative	Commons	Attribution	License,	which	permits	use,	distribution	and	reproduction	in	any	medium,	provided the original work is properly cited.©	2024	The	Authors.	Global Change Biology	published	by	John	Wiley	&	Sons	Ltd.This	article	is	a	Invited	Commentary	on	Chan	et	al.,	https://	doi.	org/	10.	1111/	gcb.	16987	.  2 of 3  |     GUIBERTto	 wild-	type	 C. proliferum	 (designated	 as	WT10).	 Following	 this	encouraging achievement, further investigations are needed to examine	the	effect	of	heat-	evolved	symbionts	 in	various	species	of	coral	and	at	different	 life	stages.	Additionally,	 long-	term	mon-itoring	 is	 essential	 to	 assess	 potential	 trade-	offs	 that	 may	 arise	from	these	interventions.	Chan	et	al.	(2023) demonstrate the suc-cess	of	heat-	evolved	 symbionts	 to	enhance	 thermal	 tolerance	 in	adult	 corals.	 In	 contrast	 to	 previous	 studies	 reporting	 failure	 in	Symbiodiniaceae	 inoculation,	 Chan	 et	 al.	 (2023) successfully es-tablished	 a	 persistent	 symbiosis	 between	 adult	 corals	 and	 heat-	evolved Symbiodiniaceae.Out	of	10	symbiont	strains	previously	tested,	SS8	derived	from	C. proliferum conferred enhanced bleaching tolerance to larvae of Acropora tenuis	(Buerger	et	al.,	2020), producing better photochem-ical efficiency, growth rate, and lower levels of extracellular reac-tive oxygen species than C. proliferum	wild	strain	WT10	(Chakravarti	et al., 2017).	To	investigate	the	effect	of	SS8	on	adult	corals,	Chan	et	 al.	 (2023) selected Galaxea fascicularis, a coral species naturally hosting both Cladocopium and Durusdinium symbionts. Two geno-types of chemically bleached G. fascicularis successfully acquired a 10-	year	 heat-	evolved	 strain	of	 the	 generalist	 species	C. proliferum (referred	to	SS8-	corals),	which	persisted	for	the	5 months	of	the	ex-periment.	As	a	comparison,	wild-	type	C. proliferum was inoculated to two genotypes of G. fascicularis	 (designated	 as	 WT10-	corals).	Combining	cutting-	edge	techniques	of	metabarcoding	and	metabo-lomics	using	matrix-	assisted	laser	desorption	ionization	mass	spec-trometry	 imaging,	 the	 effect	 of	 short-	thermal	 stress	 on	 SS8-	 and	WT10-	corals	was	assessed.Multiple studies have provided evidence that C. proliferum confers	 advantages	 to	 GBR	 corals,	 suggesting	 the	 use	 of	 this	Symbiodiniaceae as an efficient tool to enhance coral recovery after bleaching	events.	The	significance	of	heat-	evolved	C. proliferum was further	emphasized	by	Chan	et	al.	(2023)	demonstrating	that	heat-	evolved C. proliferum	 corals	 perform	better	 than	wild-	type	C. pro-liferum corals under thermal stress. This highlights the crucial role of	heat-	evolved	symbionts	 in	helping	coral	 to	withstand	heatwave	events.	 Importantly,	 SS8-	corals	 demonstrated	 high	 growth	 rates	both under elevated and ambient temperatures. This characteristic makes	heat-	evolved	C. proliferum	a	strong	candidate	for	GBR	coral	reef restoration. Metabolomics analysis conducted in this study re-vealed important differences in relative intensities of algal pigment between	SS8-	corals	and	WT10-	corals,	suggesting	that	the	thermal	tolerance	 of	 SS8-	corals	 comes	 from	 enhanced	 photoprotective	mechanisms.	SS8-	corals	also	showed	a	light	downregulation	of	me-tabolites involved in symbiosis regulation to prevent symbiont ex-pulsion,	further	supporting	the	notion	that	the	SS8	strain	confers	a	symbiosis protection face to heatwaves.Chan	et	al.	 (2023)	 is	the	first	study	to	demonstrate	that	heat-	evolved symbionts can associate with adult coral and persist long-	term	while	enhancing	coral	thermotolerance	without	a	trade-	off	 against	 growth.	 This	 study	 paves	 the	 way	 for	 utilizing	 heat-	resistant	 coral	 associated	 with	 heat-	evolved	 Symbiodiniaceae	 in	reef	restoration	projects.	If	future	studies	can	confirm	the	efficacy	of	heat-	evolved	symbionts	in	multiple	coral	species	and	their	per-formance	 on	 the	 field,	 large-	scale	 restoration	 projects	 could	 be	established.	 Going	 further,	 in-	situ	 inoculation	 of	 heat-	evolved	Symbiodiniaceae could be a viable approach to enhance coral re-silience, similar to ongoing projects using probiotic inoculation to increase	coral	 resilience.	Overall,	 the	 findings	of	 this	 study	offer	hope for the future of coral conservation and may prove vital in mitigating the damaging impacts of global change on coral reef ecosystems.AUTHOR CONTRIBUTIONSIsis Guibert: Writing – original draft; writing – review and editing.CONFLIC T OF INTERE S T S TATEMENTThe author declares no conflict of interest.DATA AVAIL ABILIT Y S TATEMENTNo data were used for this commentary.ORCIDIsis Guibert  https://orcid.org/0000-0002-6896-6659 R E FE R E N C E SAnthony,	K.	R.	N.	 (2016).	Coral	 reefs	under	 climate	change	and	ocean	acidification:	 Challenges	 and	 opportunities	 for	 management	 and	policy. Annual Review of Environment and Resources, 41,	 59–81.	https://	doi.	org/	10.	1146/	annur	ev-	envir	on-	11061	5-	085610Buerger,	P.,	Alvarez-	Roa,	C.,	Coppin,	C.	W.,	Pearce,	S.	L.,	Chakravarti,	L.	J.,	Oakeshott,	J.	G.,	Edwards,	O.	R.,	&	van	Oppen,	M.	J.	H.	(2020).	Heat-	evolved	microalgal	symbionts	increase	coral	bleaching	toler-ance. Science Advances, 6,	eaba2498.Chakravarti,	 L.	 J.	 (2019).	Manipulation of coral photosymbionts for en-hancing resilience to environmental change	(PhD	thesis).	James	Cook	University. https://	doi.	org/	10.	25903/	a7aa%	2Daa96Chakravarti,	L.	J.,	Beltran,	V.	H.,	&	van	Oppen,	M.	J.	H.	(2017).	Rapid	ther-mal	 adaptation	 in	 photosymbionts	 of	 reef-	building	 corals.	Global Change Biology, 23(11),	 4675–4688.	 https:// doi. org/ 10. 1111/ gcb. 13702 Chan,	W.	Y.,	Meyers,	 L.,	 Rudd,	D.,	 Topa,	 S.	H.,	&	 van	Oppen,	M.	 J.	H.	(2023).	Heat-	evolved	algal	symbionts	enhance	bleaching	tolerance	of	 adult	 corals	 without	 trade-	off	 against	 growth.	 Global Change Biology, 29,	6945–6968.	https://	doi.	org/	10.	1111/	gcb.	16987	Hoegh-	Guldberg,	O.,	Pendleton,	L.,	&	Kaup,	A.	 (2019).	People	and	 the	changing nature of coral reefs. Regional Studies in Marine Science, 30,	100699.	https://	doi.	org/	10.	1016/j.	rsma.	2019.	100699Hughes,	 T.	 P.,	 Kerry,	 J.	 T.,	 Baird,	 A.	 H.,	 Connolly,	 S.	 R.,	 Dietzel,	 A.,	Eakin,	 C.	M.,	Heron,	 S.	 F.,	Hoey,	 A.	 S.,	Hoogenboom,	M.	O.,	 Liu,	G.,	McWilliam,	M.	J.,	Pears,	R.	J.,	Pratchett,	M.	S.,	Skirving,	W.	J.,	Stella,	 J.	 S.,	&	Torda,	G.	 (2018).	Global	warming	 transforms	 coral	reef assemblages. Nature, 1–5,	492–496.	https://	doi.	org/	10.	1038/	s4158	6-	018-	0041-	2Intergovernmental	 Panel	 on	Climate	Change	 (IPCC).	 (2022).	The ocean and cryosphere in a changing climate.	Cambridge	University	Press.	https://	doi.	org/	10.	1017/	97810	09157964LaJeunesse,	 T.	 C.	 (2005).	 “Species”	 radiations	 of	 symbiotic	 dinoflagel-lates	 in	 the	Atlantic	 and	 Indo-	Pacific	 since	 the	Miocene-	Pliocene	transition. Molecular Biology and Evolution, 22(3),	570–581.Palacio-	Castro,	 A.	M.,	 Smith,	 T.	 B.,	 Brandtneris,	 V.,	 Snyder,	 G.	 A.,	 van	Hooidonk,	 R.,	Maté,	 J.	 L.,	Manzello,	D.,	Glynn,	 P.	W.,	 Fong,	 P.,	 &	 13652486, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17150 by University of Hong Kong, Wiley Online Library on [12/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License    |  3 of 3GUIBERTBaker,	 A.	 C.	 (2023).	 Increased	 dominance	 of	 heat-	tolerant	 sym-bionts	 creates	 resilient	 coral	 reefs	 in	 near-	term	 ocean	 warming.	Proceedings of the National Academy of Sciences of the United States of America, 120(8),	 e2202388120.	 https:// doi. org/ 10. 1073/ pnas. 22023	88120	Peixoto,	R.	S.,	Sweet,	M.,	Villela,	H.	D.	M.,	Cardoso,	P.,	Thomas,	T.,	Voolstra,	C.	 R.,	 Høj,	 L.,	 &	 Bourne,	 D.	 G.	 (2021).	 Coral	 probiotics:	 Premise,	promise, prospect. Annual Review of Animal Biosciences, 9,	265–288.	https://	doi.	org/	10.	1146/	annur	ev-	anima	l-	09012	0-	115444Quigley,	K.	M.,	Alvarez-	Roa,	C.,	Raina,	J.	B.,	Pernice,	M.,	&	van	Oppen,	M.	J.	H.	 (2023).	Heat-	evolved	microalgal	 symbionts	 increase	 thermal	bleaching	 tolerance	of	coral	 juveniles	without	a	 trade-	off	against	growth. Coral Reefs, 42, 1227–1232. https:// doi. org/ 10. 1007/ s0033	8-	023-	02426	-	zvan	Oppen,	M.	J.	H.,	Oliver,	J.	K.,	Putnam,	H.	M.,	&	Gates,	R.	D.	(2015).	Building coral reef resilience through assisted evolution. Proceedings of the National Academy of Sciences of the United States of America, 112(8),	2307–2313.	https:// doi. org/ 10. 1073/ pnas. 14223 01112 How to cite this article: Guibert,	I.	(2024).	Assisted	evolution	of algal symbionts to enhance coral reef bleaching tolerance: A	success	story.	Global Change Biology, 30, e17150. https://doi.org/10.1111/gcb.17150 13652486, 2024, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/gcb.17150 by University of Hong Kong, Wiley Online Library on [12/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License

Assisted evolution of algal symbionts to enhance coral reef bleaching tolerance: A success story

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Assisted evolution of algal symbionts to enhance coral reef bleaching tolerance: A success story

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