Editing Chloroplast (section)

== Secondary and tertiary chloroplast lineages ==

=== Green algal derived chloroplasts ===
[[Green algae]] have been taken up by many groups in three or four separate events.<ref name="Rogers-2007">{{cite journal | vauthors=Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ | title=The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of chlorarachniophyte and euglenid secondary endosymbionts | journal=Molecular Biology and Evolution | volume=24 | issue=1 | pages=54–62 | date=January 2007 | pmid=16990439 | doi=10.1093/molbev/msl129 | doi-access=free }}</ref> Primarily, secondary chloroplasts derived from green algae are in the [[euglenid]]s and [[chlorarachniophyte]]s. They are also found in one lineage of [[dinoflagellate]]s<ref name="Keeling-2010">{{cite journal | vauthors=Keeling PJ | title=The endosymbiotic origin, diversification and fate of plastids | journal=Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences | volume=365 | issue=1541 | pages=729–48 | date=March 2010 | pmid=20124341 | pmc=2817223 | doi=10.1098/rstb.2009.0103 }}</ref> and possibly the ancestor of the CASH lineage ([[cryptomonad]]s, [[Alveolata|alveolates]], [[stramenopile]]s and [[haptophyte]]s)<ref name="Moustafa-2009">{{cite journal | vauthors=Moustafa A, Beszteri B, Maier UG, Bowler C, Valentin K, Bhattacharya D | title=Genomic footprints of a cryptic plastid endosymbiosis in diatoms | journal=Science | volume=324 | issue=5935 | pages=1724–6 | date=June 2009 | pmid=19556510 | doi=10.1126/science.1172983 | url=https://epic.awi.de/id/eprint/20816/1/Mou2009a.pdf | bibcode=2009Sci...324.1724M | s2cid=11408339 }}</ref> Many green algal derived chloroplasts contain [[pyrenoid]]s, but unlike chloroplasts in their green algal ancestors, storage product collects in granules outside the chloroplast.<ref name="Kim-2009" />

==== Euglenophytes ====
{{See also|Euglenophyceae}}
[[File:Two Euglena.jpg|thumb|''[[Euglena]]'', a [[euglenophyte]], contains secondary chloroplasts from green algae.]]

The euglenophytes are a group of common [[flagellated]] [[protists]] that contain chloroplasts derived from a green alga.<ref name="Keeling-2004" /> Euglenophytes are the only group outside [[Diaphoretickes]] that have chloroplasts without performing [[kleptoplasty]].<ref>{{Cite journal |last1=Burki |first1=Fabien |last2=Roger |first2=Andrew J. |last3=Brown |first3=Matthew W. |last4=Simpson |first4=Alastair G.B. |date=2020-01-01 |title=The New Tree of Eukaryotes |url=https://linkinghub.elsevier.com/retrieve/pii/S0169534719302575 |journal=Trends in Ecology & Evolution |volume=35 |issue=1 |pages=43–55 |doi=10.1016/j.tree.2019.08.008 |pmid=31606140 |bibcode=2020TEcoE..35...43B |issn=0169-5347}}</ref><ref>{{Cite journal |last1=Sibbald |first1=Shannon J. |last2=Archibald |first2=John M. |date=2020-05-20 |title=Genomic Insights into Plastid Evolution |url=https://academic.oup.com/gbe/article/12/7/978/5836826 |journal=Genome Biology and Evolution |volume=12 |issue=7 |pages=978–990 |doi=10.1093/gbe/evaa096|pmid=32402068 |pmc=7348690 }}</ref> Euglenophyte chloroplasts have three membranes. It is thought that the membrane of the primary endosymbiont host was lost (e.g. the green algal membrane), leaving the two cyanobacterial membranes and the secondary host's phagosomal membrane.<ref name="Keeling-2004" /> Euglenophyte chloroplasts have a [[pyrenoid]] and [[thylakoid]]s stacked in groups of three. The carbon fixed through photosynthesis is stored in the form of [[paramylon]], which is contained in membrane-bound granules in the cytoplasm of the euglenophyte.<ref name="Kim-2009" /><ref name="Keeling-2010" />

==== Chlorarachniophytes ====
{{See also|Chlorarachniophyte}}
[[File:Chlorarachnion reptans.jpg|thumb|left|''[[Chlorarachnion reptans]]'' is a chlorarachniophyte. Chlorarachniophytes replaced their original [[red algal]] endosymbiont with a [[green alga]].]]

[[Chlorarachniophytes]] are a rare group of organisms that also contain chloroplasts derived from green algae,<ref name="Keeling-2004" /> though their story is more complicated than that of the euglenophytes. The ancestor of chlorarachniophytes is thought to have been a eukaryote with a ''red'' algal derived chloroplast. It is then thought to have lost its first red algal chloroplast, and later engulfed a green alga, giving it its second, green algal derived chloroplast.<ref name="Keeling-2010" />

Chlorarachniophyte chloroplasts are bounded by four membranes, except near the cell membrane, where the chloroplast membranes fuse into a double membrane.<ref name="Kim-2009" /> Their thylakoids are arranged in loose stacks of three.<ref name="Kim-2009" /> Chlorarachniophytes have a form of polysaccharide called [[chrysolaminarin]], which they store in the cytoplasm,<ref name="Keeling-2010" /> often collected around the chloroplast [[pyrenoid]], which bulges into the cytoplasm.<ref name="Kim-2009" />

Chlorarachniophyte chloroplasts are notable because the green alga they are derived from has not been completely broken down—its nucleus still persists as a [[nucleomorph]]<ref name="Keeling-2004" /> found between the second and third chloroplast membranes<ref name="Kim-2009" />—the [[periplastid space]], which corresponds to the green alga's cytoplasm.<ref name="Keeling-2010" />

==== Prasinophyte-derived chloroplast ====
{{See also|Lepidodinium}}
[[File:Lepidodinium chlorophorum 68163.jpg|thumb|left|Lepidodinium chlorophorum's green colour is caused by a plastid derived from [[Pedinophyceae]].]]

Dinoflagellates in the genus ''[[Lepidodinium]]'' have lost their original peridinin chloroplast and replaced it with a green algal derived chloroplast (more specifically, a [[prasinophyte]]).<ref name="Kim-2009" /><ref name="Hackett-2004" /> ''Lepidodinium'' is the only dinoflagellate that has a chloroplast that's not from the [[rhodoplast]] lineage. The chloroplast is surrounded by two membranes and has no nucleomorph—all the nucleomorph genes have been transferred to the dinophyte [[cell nucleus|nucleus]].<ref name="Hackett-2004" /> The endosymbiotic event that led to this chloroplast was serial secondary endosymbiosis rather than tertiary endosymbiosis—the endosymbiont was a [[green alga]] containing a primary chloroplast (making a secondary chloroplast).<ref name="Keeling-2010" />

==== Tripartite symbiosis ====
[[File:Abg4102.F1.large.jpg|thumb|left|Pseudoblepharisma tenue with its two photosynthetic symbionts.]]

The [[ciliate]] ''[[Pseudoblepharisma tenue]]'' has two bacterial symbionts, one pink, one green. In 2021, both symbionts were confirmed to be photosynthetic: Ca. ''[[Thiodictyon]] intracellulare'' ([[Chromatiaceae]]), a [[purple sulfur bacteria|purple sulfur bacterium]] with a genome just half the size of their closest known relatives; and ''[[Chlorella]]'' sp. K10, a green alga.<ref>{{cite journal | pmc=10063809 | date=2023 | last1=Christian | first1=R. | last2=Labbancz | first2=J. | last3=Usadel | first3=B. | last4=Dhingra | first4=A. | title=Understanding protein import in diverse non-green plastids | journal=Frontiers in Genetics | volume=14 | doi=10.3389/fgene.2023.969931 | doi-access=free | pmid=37007964 }}</ref> There is also a variant of ''Pseudoblepharisma tenue'' that only contains chloroplasts from green algae and no endosymbiotic purple bacteria.<ref name="Hines">{{cite journal |last1=Hines |first1=Hunter N. |last2=McCarthy |first2=Peter J. |last3=Esteban |first3=Genoveva F. |title=A Case Building Ciliate in the Genus Pseudoblepharisma Found in Subtropical Fresh Water |journal=Diversity |date=27 February 2022 |volume=14 |issue=3 |pages=174 |doi=10.3390/d14030174 |doi-access=free|bibcode=2022Diver..14..174H }}</ref>

=== Red algal derived chloroplasts ===
Secondary chloroplasts derived from [[red algae]] appear to have only been taken up only once, which then diversified into a large group called [[chromist]]s or chromalveolates. Today they are found in the [[Haptophyte|haptophytes]], [[Cryptomonad|cryptomonads]], [[Stramenopile|heterokonts]], [[Dinoflagellate|dinoflagellates]] and [[Apicomplexa|apicomplexans]] (the CASH lineage).<ref name="Keeling-2010" /> Red algal secondary chloroplasts usually contain chlorophyll c and are surrounded by four membranes.<ref name="Kim-2009" />

However, chromist [[monophyly]] has been rejected, and it is considered more likely that some chromists acquired their plastids by incorporating another chromist instead of inheriting them from a common ancestor. [[Cryptophyte]]s seem to have acquired plastids from red algae, which were then transmitted from them to both the [[Ochrophyte|Heterokontophyte]]s and the [[Haptophyte]]s, and then from these last to the [[Myzozoa]].<ref name="Strassert Irisarri Williams Burki 2021">{{Cite journal |last1=Strassert |first1=Jürgen F. H. |last2=Irisarri |first2=Iker |last3=Williams |first3=Tom A. |last4=Burki |first4=Fabien |date=2021-03-25 |title=A molecular timescale for eukaryote evolution with implications for the origin of red algal-derived plastids |journal=Nature Communications |volume=12 |issue=1 |pages=1879 |doi=10.1038/s41467-021-22044-z |pmid=33767194 |pmc=7994803 |bibcode=2021NatCo..12.1879S |issn=2041-1723}}</ref>

==== Cryptophytes ====
{{See also|Cryptomonad}}
[[File:CSIRO ScienceImage 6743 SEM Cryptophyte.jpg|thumb|Cryptophytes under [[Scanning electron microscope|SEM]].]]

[[Cryptomonad|Cryptophytes]], or cryptomonads, are a group of algae that contain a red-algal derived chloroplast. Cryptophyte chloroplasts contain a [[nucleomorph]] that superficially resembles that of the [[chlorarachniophytes]].<ref name="Keeling-2004" /> Cryptophyte chloroplasts have four membranes. The outermost membrane is continuous with the [[rough endoplasmic reticulum]]. They synthesize ordinary [[starch]], which is stored in granules found in the periplastid space—outside the original double membrane, in the place that corresponds to the ancestral red alga's cytoplasm. Inside cryptophyte chloroplasts is a [[pyrenoid]] and [[thylakoid]]s in stacks of two.<ref name="Kim-2009" /> Cryptophyte chloroplasts do not have [[phycobilisome]]s,<ref name="Kim-2009" /> but they do have [[Phycobilin|phycobilin pigments]] which they keep in the thylakoid space, rather than anchored on the outside of their thylakoid membranes.<ref name="Kim-2009" /><ref name="Keeling-2004" />

Cryptophytes may have played a key role in the spreading of red algal based chloroplasts.<ref>{{Cite thesis|last=Toledo|first=Rafael Isaac Ponce| name-list-style=vanc |title=Origins and early evolution of photosynthetic eukaryotes|date=5 March 2018|publisher=Université Paris-Saclay|url=https://tel.archives-ouvertes.fr/tel-01760725|language=en}}</ref><ref>{{cite journal | vauthors=Bodył A | title=Did some red alga-derived plastids evolve via kleptoplastidy? A hypothesis | journal=Biological Reviews of the Cambridge Philosophical Society | volume=93 | issue=1 | pages=201–222 | date=February 2018 | pmid=28544184 | doi=10.1111/brv.12340 | s2cid=24613863 }}</ref>

==== Haptophytes ====
{{See also|Haptophyte}}
[[File:Gephyrocapsa oceanica brighter.jpg|thumb|left|[[Scanning electron micrograph]] of ''[[Gephyrocapsa oceanica]]'', a haptophyte.]]

[[Haptophytes]] are similar and closely related to cryptophytes or heterokontophytes.<ref name="Keeling-2010" /> Their chloroplasts lack a nucleomorph,<ref name="Kim-2009" /><ref name="Keeling-2004" /> their thylakoids are in stacks of three, and they synthesize [[chrysolaminarin]] sugar, which are stored in granules completely outside of the chloroplast, in the cytoplasm of the haptophyte.<ref name="Kim-2009" />

==== Stramenopiles <span style="font-weight: 400;">(heterokontophytes)</span> ====
{{See also|Stramenopile}}[[File:20110123 185042 Diatom.jpg|thumb|upright=0.8|The photosynthetic pigments present in their chloroplasts make [[diatoms]] greenish-brown.]]

The [[stramenopile]]s, also known as heterokontophytes, are a very large and diverse group of eukaryotes. It inlcludes [[Ochrophyta]]—which includes [[diatoms]], [[brown algae]] (seaweeds), and [[golden algae]] (chrysophytes)<ref name="Campbell-2009f" />— and [[Yellow-green algae|Xanthophyceae]] (also called yellow-green algae).<ref name="Keeling-2010" />

Heterokont chloroplasts are very similar to haptophyte chloroplasts. They have a [[pyrenoid]], triplet thylakoids, and, with some exceptions,<ref name="Kim-2009" /> four layer plastidic envelope with the outermost membrane connected to the [[endoplasmic reticulum]]. Like haptophytes, stramenopiles store sugar in [[chrysolaminarin]] granules in the cytoplasm.<ref name="Kim-2009" /> Stramenopile chloroplasts contain [[chlorophyll a|chlorophyll ''a'']] and, with a few exceptions,<ref name="Kim-2009" /> [[Chlorophyll c|chlorophyll ''c'']].<ref name="Keeling-2004" /> They also have [[carotenoid]]s which give them their many colors.<ref name="Campbell-2009f" />

==== Apicomplexans, chromerids, and dinophytes ====
{{See also|Alveolate|Myzozoa}}
The alveolates are a major clade of unicellular eukaryotes of both [[Autotroph|autotrophic]] and [[Heterotroph|heterotrophic]] members. Many members contain a red-algal derived plastid. One notable characteristic of this diverse group is the frequent loss of photosynthesis. However, a majority of these heterotrophs continue to process a non-photosynthetic plastid.<ref name="Janouškovec-2017">{{cite journal | vauthors=Janouškovec J, Gavelis GS, Burki F, Dinh D, Bachvaroff TR, Gornik SG, Bright KJ, Imanian B, Strom SL, Delwiche CF, Waller RF, Fensome RA, Leander BS, Rohwer FL, Saldarriaga JF | display-authors=6 | title=Major transitions in dinoflagellate evolution unveiled by phylotranscriptomics | journal=Proceedings of the National Academy of Sciences of the United States of America | volume=114 | issue=2 | pages=E171–E180 | date=January 2017 | pmid=28028238 | pmc=5240707 | doi=10.1073/pnas.1614842114 | bibcode=2017PNAS..114E.171J | doi-access=free }}</ref>

===== Apicomplexans =====
[[File:Plasmodium.png|thumb|Diagram of Plasmodium, including its apicoplast.]]

[[Apicomplexans]] are a group of alveolates. Like the [[helicosproidia]], they're parasitic, and have a nonphotosynthetic chloroplast.<ref name="Keeling-2010" /> They were once thought to be related to the helicosproidia, but it is now known that the helicosproida are green algae rather than part of the CASH lineage.<ref name="Keeling-2010" /> The apicomplexans include ''[[Plasmodium]]'', the [[malaria]] parasite. Many apicomplexans keep a [[vestigial]] red algal derived chloroplast<ref name="Nair-2011" /><ref name="Keeling-2010" /> called an [[apicoplast]], which they inherited from their ancestors. Apicoplasts have lost all photosynthetic function, and contain no photosynthetic pigments or true thylakoids. They are bounded by four membranes, but the membranes are not connected to the [[endoplasmic reticulum]].<ref name="Kim-2009" /> Other apicomplexans like ''[[Cryptosporidium]]'' have lost the chloroplast completely.<ref name="Nair-2011" /> Apicomplexans store their energy in [[amylopectin]] granules that are located in their cytoplasm, even though they are nonphotosynthetic.<ref name="Kim-2009" />

The fact that apicomplexans still keep their nonphotosynthetic chloroplast around demonstrates how the chloroplast carries out important functions other than [[photosynthesis]]. [[Plant]] chloroplasts provide plant cells with many important things besides sugar, and apicoplasts are no different—they synthesize [[fatty acid]]s, [[isopentenyl pyrophosphate]], [[iron-sulfur clusters]], and carry out part of the [[heme]] pathway.<ref name="Nair-2011" /> The most important apicoplast function is [[isopentenyl pyrophosphate]] synthesis—in fact, apicomplexans die when something interferes with this apicoplast function, and when apicomplexans are grown in an isopentenyl pyrophosphate-rich medium, they dump the organelle.<ref name="Nair-2011" />

===== Chromerids =====
[[File:Vitrella brassicaformis LM Michalek 2020.png|thumb|Typical life cycle stages of [[Vitrella brassicaformis]], a chromerid.]]

The [[chromerid]]s are a group of algae known from Australian corals which comprise some close photosynthetic relatives of the apicomplexans. The first member, ''[[Chromera velia]]'', was discovered and first isolated in 2001. The discovery of ''Chromera velia'' with similar structure to the apicomplexans, provides an important link in the evolutionary history of the apicomplexans and dinophytes. Their plastids have four membranes, lack chlorophyll c and use the type II form of [[RuBisCO]] obtained from a horizontal transfer event.<ref>{{cite journal | vauthors=Quigg A, Kotabová E, Jarešová J, Kaňa R, Setlík J, Sedivá B, Komárek O, Prášil O | display-authors=6 | title=Photosynthesis in Chromera velia represents a simple system with high efficiency | journal=PLOS ONE | volume=7 | issue=10 | pages=e47036 | date=10 October 2012 | pmid=23071705 | pmc=3468483 | doi=10.1371/journal.pone.0047036 | bibcode=2012PLoSO...747036Q | doi-access=free }}</ref>

===== Dinophytes =====
[[File:Ceratium furca.jpg|thumb|''[[Ceratium furca]]'', a [[peridinin]]-containing dinophyte.<ref>{{cite journal  |vauthors=Meeson BW, Chang SS, Sweeney BM |doi=10.1515/botm.1982.25.8.347 |title=Characterization of Peridinin-Chlorophyll α-Proteins from the Marine Dinoflagellate Ceratium furca |year=1982 |journal=Botanica Marina |volume=25 |issue=8 |pages=347–50|bibcode=1982BoMar..25..347M |s2cid=83867103 }}</ref>]]

The [[dinoflagellates]] are yet another very large and diverse group, around half of which are at least partially photosynthetic (i.e. [[Mixotroph|mixotrophic]]).<ref name="Campbell-2009f" /><ref name="Hackett-2004">{{cite journal | vauthors=Hackett JD, Anderson DM, Erdner DL, Bhattacharya D | title=Dinoflagellates: a remarkable evolutionary experiment | journal=American Journal of Botany | volume=91 | issue=10 | pages=1523–34 | date=October 2004 | pmid=21652307 | doi=10.3732/ajb.91.10.1523 }}</ref> Dinoflagellate chloroplasts have relatively complex history. Most dinoflagellate chloroplasts are secondary [[red algae|red algal]] derived chloroplasts. Many dinoflagellates have lost the chloroplast (becoming nonphotosynthetic), some of these have replaced it though ''tertiary'' endosymbiosis.<ref name="Dorrell-2011">{{cite journal | vauthors=Dorrell RG, Smith AG | title=Do red and green make brown?: perspectives on plastid acquisitions within chromalveolates | journal=Eukaryotic Cell | volume=10 | issue=7 | pages=856–68 | date=July 2011 | pmid=21622904 | pmc=3147421 | doi=10.1128/EC.00326-10 }}</ref> Others replaced their original chloroplast with a [[green algae|green algal]] derived chloroplast.<ref name="Keeling-2004" /><ref name="Keeling-2010" /><ref name="Hackett-2004" /> The peridinin chloroplast is thought to be the dinophytes' "original" chloroplast,<ref name="Hackett-2004" /> which has been lost, reduced, replaced, or has company in several other dinophyte lineages.<ref name="Keeling-2010" />

The most common dinophyte chloroplast is the [[peridinin]]-type chloroplast, characterized by the [[carotenoid]] pigment [[peridinin]] in their chloroplasts, along with [[chlorophyll a|chlorophyll ''a'']] and [[chlorophyll c2|chlorophyll ''c''<sub>2</sub>]].<ref name="Keeling-2004" /><ref name="Hackett-2004" /> Peridinin is not found in any other group of chloroplasts.<ref name="Hackett-2004" /> The peridinin chloroplast is bounded by three membranes (occasionally two),<ref name="Kim-2009" /> having lost the red algal endosymbiont's original cell membrane.<ref name="Keeling-2004" /><ref name="Keeling-2010" /> The outermost membrane is not connected to the endoplasmic reticulum.<ref name="Kim-2009" /><ref name="Hackett-2004" /> They contain a [[pyrenoid]], and have triplet-stacked thylakoids. Starch is found outside the chloroplast.<ref name="Kim-2009" /> Peridinin chloroplasts also have DNA that is highly [[genome reduction|reduced]] and fragmented into many small circles.<ref name="Hackett-2004" /> Most of the genome has migrated to the nucleus, and only critical photosynthesis-related genes remain in the chloroplast. 

Most dinophyte chloroplasts contain form II RuBisCO, at least the [[photosynthetic pigments]] [[chlorophyll a|chlorophyll ''a'']], [[chlorophyll c2|chlorophyll ''c<sub>2</sub>'']], [[beta-carotene|''beta''-carotene]], and at least one dinophyte-unique [[xanthophyll]] ([[peridinin]], [[dinoxanthin]], or [[diadinoxanthin]]), giving many a golden-brown color.<ref name="Janouškovec-2017" /><ref name="Hackett-2004" /> All dinophytes store starch in their cytoplasm, and most have chloroplasts with thylakoids arranged in stacks of three.<ref name="Kim-2009" />

=== Haptophyte-derived chloroplasts ===
[[File:Karenia brevis.jpg|thumb|upright|''[[Karenia brevis]]'' is a [[fucoxanthin]]-containing dynophyte responsible for [[algal bloom]]s called "[[red tide]]s".<ref name="Hackett-2004" />]]

The [[fucoxanthin]] dinophyte lineages (including ''[[Karlodinium]]'' and ''[[Karenia (dinoflagellate)|Karenia]]'')<ref name="Keeling-2010" /> lost their original red algal derived chloroplast, and replaced it with a new chloroplast derived from a [[haptophyte]] endosymbiont, making these tertiary plastids. ''[[Karlodinium]]'' and ''[[Karenia (dinoflagellate)|Karenia]]'' probably took up different endosymbionts.<ref name="Keeling-2010" /> Because the haptophyte chloroplast has four membranes, tertiary endosymbiosis would be expected to create a six membraned chloroplast, adding the haptophyte's [[cell membrane]] and the dinophyte's [[phagosomal vacuole]].<ref name="Tengs-2000" /> However, the haptophyte was heavily reduced, stripped of a few membranes and its nucleus, leaving only its chloroplast (with its original double membrane), and possibly one or two additional membranes around it.<ref name="Keeling-2010" /><ref name="Tengs-2000">{{cite journal | vauthors=Tengs T, Dahlberg OJ, Shalchian-Tabrizi K, Klaveness D, Rudi K, Delwiche CF, Jakobsen KS | title=Phylogenetic analyses indicate that the 19'Hexanoyloxy-fucoxanthin-containing dinoflagellates have tertiary plastids of haptophyte origin | journal=Molecular Biology and Evolution | volume=17 | issue=5 | pages=718–29 | date=May 2000 | pmid=10779532 | doi=10.1093/oxfordjournals.molbev.a026350 | author-link4=Dag Klaveness (limnologist) | doi-access=free }}</ref>

Fucoxanthin-containing chloroplasts are characterized by having the pigment [[fucoxanthin]] (actually [[19′-hexanoyloxy-fucoxanthin]] and/or [[19′-butanoyloxy-fucoxanthin]]) and no peridinin. Fucoxanthin is also found in haptophyte chloroplasts, providing evidence of ancestry.<ref name="Hackett-2004" />

=== Diatom-derived chloroplasts ===
[[File:Durinskia baltica.jpg|thumb|Durinskia is a genus significant to the study of endosymbiotic events and organelle integration.<ref name="Zerdoner2017">{{cite journal | vauthors = Žerdoner Čalasan A, Kretschmann J, Gottschling M | title = Absence of co-phylogeny indicates repeated diatom capture in dinophytes hosting a tertiary endosymbiont. | journal = Organisms Diversity & Evolution | date = March 2018 | volume = 18 | issue = 1 | pages = 29–38 | doi = 10.1007/s13127-017-0348-0 | s2cid = 3830963 }}</ref>]]

Some dinophytes, like ''[[Kryptoperidinium]]'' and ''[[Durinskia]]'',<ref name="Keeling-2010" /> have a [[diatom]] ([[heterokontophyte]])-derived chloroplast.<ref name="Keeling-2004" /> These chloroplasts are bounded by up to ''five'' membranes,<ref name="Keeling-2004" /> (depending on whether the entire diatom endosymbiont is counted as the chloroplast, or just the red algal derived chloroplast inside it). The diatom endosymbiont has been reduced relatively little—it still retains its original [[Mitochondrion|mitochondria]],<ref name="Keeling-2010" /> and has [[endoplasmic reticulum]], [[ribosome]]s, a [[cell nucleus|nucleus]], and of course, red algal derived chloroplasts—practically a complete [[cell (biology)|cell]],<ref name="Schnepf-1999">{{cite journal | vauthors=Schnepf E, Elbrächter M |doi=10.1080/00173139908559217 |title=Dinophyte chloroplasts and phylogeny – A review |year=1999 |journal=Grana |volume=38 |issue=2–3 |pages=81–97|doi-access=free |bibcode=1999Grana..38...81S }}</ref> all inside the host's [[endoplasmic reticulum lumen]].<ref name="Keeling-2010" /> However the diatom endosymbiont can't store its own food—its storage polysaccharide is found in granules in the dinophyte host's cytoplasm instead.<ref name="Kim-2009" /><ref name="Schnepf-1999" /> The diatom endosymbiont's nucleus is present, but it probably can't be called a [[nucleomorph]] because it shows no sign of [[genome reduction]], and might have even been ''expanded''.<ref name="Keeling-2010" /> Diatoms have been engulfed by dinoflagellates at least three times.<ref name="Keeling-2010" />

The diatom endosymbiont is bounded by a single membrane,<ref name="Hackett-2004" /> inside it are chloroplasts with four membranes. Like the diatom endosymbiont's diatom ancestor, the chloroplasts have triplet thylakoids and [[pyrenoid]]s.<ref name="Schnepf-1999" />

In some of these [[genera]], the diatom endosymbiont's chloroplasts aren't the only chloroplasts in the dinophyte. The original three-membraned peridinin chloroplast is still around, converted to an [[Eyespot apparatus|eyespot]].<ref name="Keeling-2004" /><ref name="Keeling-2010" />

=== Kleptoplasty ===
{{Main|Kleptoplasty}}


In some groups of [[mixotrophic]] [[protist]]s, like some [[dinoflagellate]]s (e.g. ''[[Dinophysis]]''), chloroplasts are separated from a captured alga and used temporarily. These [[kleptoplasty|klepto chloroplasts]] may only have a lifetime of a few days and are then replaced.<ref name="Skovgaard-1998">{{cite journal |doi=10.3354/ame015293 |title=Role of chloroplast retention in a marine dinoflagellate |year=1998 |last1=Skovgaard |first1=Alf | name-list-style=vanc |journal=Aquatic Microbial Ecology |volume=15 |pages=293–301|doi-access=free }}</ref><ref>{{cite journal | vauthors=Dorrell RG, Howe CJ | title=Integration of plastids with their hosts: Lessons learned from dinoflagellates | journal=Proceedings of the National Academy of Sciences of the United States of America | volume=112 | issue=33 | pages=10247–54 | date=August 2015 | pmid=25995366 | pmc=4547248 | doi=10.1073/pnas.1421380112 | bibcode=2015PNAS..11210247D | doi-access=free }}</ref>

==== Cryptophyte-derived dinophyte chloroplast ====
[[File:Dinophysis acuminata.jpg|thumb|left|upright|''[[Dinophysis acuminata]]'' has chloroplasts taken from a [[cryptomonad|cryptophyte]].<ref name="Keeling-2004" />]]

Members of the genus ''[[Dinophysis]]'' have a [[phycobilin]]-containing<ref name="Tengs-2000" /> chloroplast taken from a [[cryptomonad|cryptophyte]].<ref name="Keeling-2004" /> However, the cryptophyte is not an endosymbiont—only the chloroplast seems to have been taken, and the chloroplast has been stripped of its [[nucleomorph]] and outermost two membranes, leaving just a two-membraned chloroplast. Cryptophyte chloroplasts require their nucleomorph to maintain themselves, and ''Dinophysis'' species grown in [[cell culture]] alone cannot survive, so it is possible (but not confirmed) that the ''Dinophysis'' chloroplast is a [[kleptoplast]]—if so, ''Dinophysis'' chloroplasts wear out and ''Dinophysis'' species must continually engulf cryptophytes to obtain new chloroplasts to replace the old ones.<ref name="Hackett-2004" />