Atelocyanobacterium thalassa

{{Short description|Species of bacterium}} {{Use dmy dates|date=April 2024}} {{Automatic taxobox |image = Braarudosphaera Bigelowii Nitroplast.webp|image_caption=Black arrow: the nitroplast inside ''B. bigelowii'' (motile phase) | name = ''Candidatus'' Atelocyanobacterium thalassa | taxon = Atelocyanobacterium | species_text = {{nowrap|'''''Ca.'' Atelocyanobacterium thalassa'''}} | binomial_text = ''Candidatus'' Atelocyanobacterium thalassa | authority = Thompson et al., 2012<ref name="Thompson_2012"/> | synonyms = * UCYN-A * Nitroplast }}

'''''Candidatus'' Atelocyanobacterium thalassa''', also referred to as '''UCYN-A''', is a nitrogen-fixing species of cyanobacteria that exists exclusively as an obligate symbiont. Despite being found in measurable quantities throughout the world's oceans, ''A. thalassa'' is not known to be free-living in any environment.<ref name="Thompson_2012">{{cite journal | vauthors = Thompson AW, Foster RA, Krupke A, Carter BJ, Musat N, Vaulot D, Kuypers MM, Zehr JP | display-authors = 6 | title = Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga | journal = Science | volume = 337 | issue = 6101 | pages = 1546–1550 | date = September 2012 | pmid = 22997339 | doi = 10.1126/science.1222700 | s2cid = 7071725 | bibcode = 2012Sci...337.1546T }}</ref><ref name="Turk-Kubo_2017">{{cite journal |vauthors=Turk-Kubo KA, Farnelid HM, Shilova IN, Henke B, Zehr JP |date=April 2017 |title=Distinct ecological niches of marine symbiotic N2-fixing cyanobacterium ''Candidatus'' Atelocyanobacterium thalassa sublineages |url=https://escholarship.org/uc/item/3mx1x7vw |url-status=live |journal=Journal of Phycology |volume=53 |issue=2 |pages=451–461 |bibcode=2017JPcgy..53..451T |doi=10.1111/jpy.12505 |pmid=27992651 |s2cid=36662899 |archive-url=https://web.archive.org/web/20221001082623/https://escholarship.org/uc/item/3mx1x7vw |archive-date=1 October 2022 |access-date=24 January 2023|url-access=subscription }}</ref> Unlike typical cyanobacteria, its genome has undergone massive reduction, losing the genes for RuBisCO, photosystem II, and the TCA cycle.<ref name="Zehr_2016" /> Consequently, it possesses no independent means of fixing carbon or generating energy through photosynthesis, rendering it entirely dependent on its host (so far only known to be ''Braarudosphaera bigelowii'' and a closely-related unnamed species).<ref name="Zehr_2016" />

This partnership is characterized by a strict metabolic exchange: ''A. thalassa'' fixes atmospheric nitrogen into ammonium for the host, while the host provides the essential carbon products the bacterium can no longer produce for itself.<ref name="UCSC">{{cite web |date=20 September 2012 |title=Unusual symbiosis discovered in marine microorganisms |url=http://news.ucsc.edu/2012/09/symbiosis.html |url-status=live |archive-url=https://web.archive.org/web/20170710100712/https://news.ucsc.edu/2012/09/symbiosis.html |archive-date=10 July 2017 |access-date=13 January 2017 |publisher=University of California Santa Cruz Newscenter |vauthors=Stephens T}}</ref> While various sublineages are distributed across diverse marine niches—from oligotrophic open waters to coastal regions—every known version of ''A. thalassa'' remains confined within a host cell.<ref name="Turk-Kubo_2017" />

In the more integrated form, specifically the UCYN-A2 sublineage<ref>{{Cite journal |last1=Thompson |first1=Anne |last2=Carter |first2=Brandon J. |last3=Turk-Kubo |first3=Kendra |last4=Malfatti |first4=Francesca |last5=Azam |first5=Farooq |last6=Zehr |first6=Jonathan P. |date=October 2014 |title=Genetic diversity of the unicellular nitrogen-fixing cyanobacteria UCYN-A and its prymnesiophyte host: UCYN-A genetic diversity |url=https://cloudfront.escholarship.org/dist/prd/content/qt4687q7k8/qt4687q7k8.pdf?t=nx0365 |journal=Environmental Microbiology |language=en |volume=16 |issue=10 |pages=3238–3249 |doi=10.1111/1462-2920.12490 |pmid=24761991 |s2cid=24822220}}</ref> within the alga ''Braarudosphaera bigelowii'', the relationship has progressed so far that the bacterium is now considered a true organelle, termed a '''nitroplast'''.<ref name="nature.com">{{Cite journal |last=Wong |first=Carissa |date=11 April 2024 |title=Scientists discover first algae that can fix nitrogen — thanks to a tiny cell structure |url=https://www.nature.com/articles/d41586-024-01046-z |archive-url=https://web.archive.org/web/20240414144507/https://www.nature.com/articles/d41586-024-01046-z |archive-date=14 April 2024 |access-date=16 April 2024 |journal=Nature |volume=628 |issue=8009 |page=702 |doi=10.1038/d41586-024-01046-z |pmid=38605201 |bibcode=2024Natur.628..702W |url-access=subscription |url-status=live }}</ref><ref name="Coale_2024">{{Cite journal |last1=Coale |first1=Tyler H. |last2=Loconte |first2=Valentina |last3=Turk-Kubo |first3=Kendra A. |last4=Vanslembrouck |first4=Bieke |last5=Mak |first5=Wing Kwan Esther |last6=Cheung |first6=Shunyan |last7=Ekman |first7=Axel |last8=Chen |first8=Jian-Hua |last9=Hagino |first9=Kyoko |last10=Takano |first10=Yoshihito |last11=Nishimura |first11=Tomohiro |last12=Adachi |first12=Masao |last13=Le Gros |first13=Mark |last14=Larabell |first14=Carolyn |author14-link=Carolyn Larabell |last15=Zehr |first15=Jonathan P. |date=12 April 2024 |title=Nitrogen-fixing organelle in a marine alga |journal=Science |volume=384 |issue=6692 |pages=217–222 |doi=10.1126/science.adk1075 |pmid=38603509 |bibcode=2024Sci...384..217C |url=https://www.jzehrlab.com/publications}}</ref>{{efn|Contrary to what the ''-plast'' suffix may imply, the organelle is not a derived form of the plastid.}} In these cases, the "bacterium" is imported with nuclear-encoded proteins and its division is synchronized with the host, mirroring the evolutionary history of mitochondria and chloroplasts.<ref name="nature.com" /> This discovery of the first nitrogen-fixing organelle in a eukaryote has major implications for agricultural science, as it demonstrates a biological pathway for potentially engineering crops that do not require nitrogen fertilizer.<ref name="nature.com" />

Members of ''A. thalassa'' are spheroid in shape and are 1-2 μm in diameter,<ref name= Hagino >{{Cite journal |last1=Hagino |first1=Kyoko |last2=Onuma |first2=Ryo |last3=Kawachi |first3=Masanobu |last4=Horiguchi |first4=Takeo |date=4 December 2013 |title=Discovery of an Endosymbiotic Nitrogen-Fixing Cyanobacterium UCYN-A in ''Braarudosphaera bigelowii'' (Prymnesiophyceae) |journal=PLOS ONE |volume=8 |issue=12 |article-number=e81749 |doi=10.1371/journal.pone.0081749 |issn=1932-6203 |pmc=3852252 |pmid=24324722|bibcode=2013PLoSO...881749H |doi-access=free }}</ref> and provide nitrogen to ocean regions by fixing non biologically available atmospheric nitrogen into biologically available ammonium that other marine microorganisms can use.<ref name="Thompson_2012" /> There are many sublineages of ''A. thalassa'' that are distributed across a wide range of marine environments and host organisms.<ref name="Turk-Kubo_2017" /> It appears that some sublineages of ''A. thalassa'' have a preference for oligotrophic ocean waters while other sublineages prefer coastal waters.<ref name=":1" /> Much is still unknown about all of ''A. thalassa''<nowiki/>'s hosts and host preferences.<ref name="Thompson_2012" />

== Discovery == In 1998, Jonathan Zehr, an ocean ecologist at the University of California, Santa Cruz, and his colleagues found an unknown DNA sequence that appeared to be for an unknown nitrogen-fixing cyanobacterium in the Pacific Ocean, which they called UCYN-A (unicellular cyanobacterial group A).<ref name="Zehr, Mellon, Zani">{{cite journal |last1=Zehr |first1=Jonathan P. |last2=Mellon |first2=Mark T. |last3=Zani |first3=Sabino |title=New nitrogen-fixing microorganisms detected in oligotrophic oceans by amplification of nitrogenase (''nifH'') genes |journal=Applied and Environmental Microbiology |date=September 1998 |volume=64 |issue=9 |pages=3444–3450 |doi=10.1128/AEM.64.9.3444-3450.1998|pmid=9726895 |pmc=106745 |bibcode=1998ApEnM..64.3444Z }} Correction to the above article {{cite journal |title=Authors and title as above |date=December 1998 |journal=Applied and Environmental Microbiology |volume=64 |issue=12 | page=5067 |pmid=16349571 |doi=10.1128/AEM.64.12.5067-5067.1998 |pmc=90973 | bibcode=1998ApEnM..64.5067Z}}</ref> At the same time, Kyoko Hagino, a paleontologist at Kochi University, was working to culture the host organism, ''B. bigelowii''.<ref>{{Cite web |last=Ralls |first=Eric |title=Introducing the "nitroplast" -- The first nitrogen-fixing organelle |url=https://www.earth.com/news/nitroplast-discovery-first-nitrogen-fixing-organelle/ |access-date=2024-04-21 |website=Earth.com |language=en}}</ref>{{r|Hagino}}

== Ecology ==

=== Nitrogen fixation === Nitrogen fixation, which is the reduction of N2 to biologically available nitrogen, is an important source of N for aquatic ecosystems. For many decades, N2 fixation was vastly underestimated.{{Citation needed|date=May 2022}} The assumption that N2 fixation only occurred via ''Trichodesmium'' and ''Richelia'' led to the conclusion that in the oceans, nitrogen output exceeded the input.{{Citation needed|date=May 2022}} However, researchers found that the nitrogenase complex has variable evolutionary histories.{{Citation needed|date=May 2022}} The use of the polymerase chain reaction (PCR), removed the requirement of cultivation or microscopy to identify N2 fixing microorganisms. As a result, marine N2-fixing microorganisms other than ''Trichodesimum'' were found by sequencing PCR-amplified fragments of the gene nitrogenase (''nifH''). Nitrogenase is the enzyme that catalyzes nitrogen fixation, and studies have shown that ''nifH'' is widely distributed throughout the different parts of the ocean.<ref name= Zehr >{{cite book |vauthors=Zehr JP, Turner PJ |series=Methods in Microbiology |volume=30 |title=Marine Microbiology |date=1 January 2001 |chapter=Nitrogen fixation: Nitrogenase genes and gene expression |language=en |publisher=Academic Press |pages=271–286 |doi=10.1016/s0580-9517(01)30049-1 |isbn=978-0-12-521530-5}}</ref>

In 1989, a short ''nifH'' gene sequence was discovered,{{Citation needed|date=May 2022}} and 15 years later it was revealed to be an unusual cyanobacterium that is widely distributed.<ref>{{cite journal | vauthors = Zehr JP, McReynolds LA | title = Use of degenerate oligonucleotides for amplification of the ''nifH'' gene from the marine cyanobacterium ''Trichodesmium thiebautii'' | journal = Applied and Environmental Microbiology | volume = 55 | issue = 10 | pages = 2522–2526 | date = October 1989 | pmid = 2513774 | doi = 10.1128/aem.55.10.2522-2526.1989 | pmc = 203115 | bibcode = 1989ApEnM..55.2522Z }}</ref> The microbe was originally given the name UCYN-A for "unicellular cyanobacteria group A". In research published in 1998, ''nifH'' sequences were amplified directly from water collected in the Pacific and Atlantic Oceans, and shown to be from bacterial, unicellular cyanobacterial ''nifH'', ''Trichodesmium'' and diatom symbionts.{{r|Zehr, Mellon, Zani}} With the use of cultivation-independent PCR and quantitative PCR (qPCR) targeting the ''nifH'' gene, studies found that ''A. thalassa'' is distributed in many ocean regions, showing that the oceanic plankton contain a broader range of nitrogen-fixing microorganisms than was previously believed.

=== Habitat === thumb|Global distribution of ''A. thalassa''<ref name=":0" />|359x359pxThe distribution of ''A. thalassa'' is cosmopolitan and is found throughout the world's oceans including the North Sea, Mediterranean Sea, Adriatic Sea, Red Sea, Arabian Sea, South China Sea, and the Coral Sea.,<ref name=":0" /> further reinforcing its significant role in nitrogen fixation.<ref name=":0" /> Although ''A. thalassa'' is ubiquitous, its abundance is highly regulated by various abiotic factors such as temperature and nutrients.<ref>{{cite journal | vauthors = Goebel NL, Turk KA, Achilles KM, Paerl R, Hewson I, Morrison AE, Montoya JP, Edwards CA, Zehr JP | display-authors = 6 | title = Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean | journal = Environmental Microbiology | volume = 12 | issue = 12 | pages = 3272–3289 | date = December 2010 | pmid = 20678117 | doi = 10.1111/j.1462-2920.2010.02303.x | bibcode = 2010EnvMi..12.3272G }}</ref> Studies have shown that it occupies cooler waters compared to other diazotrophs.<ref>{{cite journal | vauthors = Moisander PH, Beinart RA, Hewson I, White AE, Johnson KS, Carlson CA, Montoya JP, Zehr JP | display-authors = 6 | title = Unicellular cyanobacterial distributions broaden the oceanic N2 fixation domain | journal = Science | volume = 327 | issue = 5972 | pages = 1512–1514 | date = March 2010 | pmid = 20185682 | doi = 10.1126/science.1185468 | bibcode = 2010Sci...327.1512M | s2cid = 206524855 | doi-access = free }}</ref>

There are four main defined sublineages of ''A. thalassa,'' namely, UCYN-A1, UCYN-A2, UCYN-A3, and UCYN-A4 (see § Diversity below); studies have shown that these groups are adapted to different marine environments.<ref name="Turk-Kubo_2017" /> UCYN-A1 and UCYN-A3 co-exist in open-ocean oligotrophic waters. while UCYN-A2 and UCYN-A4 co-exist in coastal waters.<ref name="Turk-Kubo_2017" /><ref name=":1">{{cite journal | vauthors = Cabello AM, Turk-Kubo KA, Hayashi K, Jacobs L, Kudela RM, Zehr JP | title = Unexpected presence of the nitrogen-fixing symbiotic cyanobacterium UCYN-A in Monterey Bay, California | journal = Journal of Phycology | volume = 56 | issue = 6 | pages = 1521–1533 | date = December 2020 | pmid = 32609873 | pmc = 7754506 | doi = 10.1111/jpy.13045 | bibcode = 2020JPcgy..56.1521C }}</ref> UCYN-A2 is typically found in high latitude temperate coastal waters. In addition, it can also be found co-occurring with UCYN-A4 in the coastal bodies of water. UCYN-A3 was found to be in greater abundance in the surface of the open ocean in the subtropics. In addition, UCYN-A3 has only been found to co-occur with UCYN-A1 thus far.

== Metabolism ==

=== Obligate photoheterotroph === ''Atelocyanobacterium thalassa'' is categorized as a photoheterotroph. Complete genome analysis reveals a reduced-size genome of 1.44 megabases, and the lack of pathways needed for metabolic self-sufficiency common to cyanobacteria.<ref name="Tripp_2010">{{cite journal |display-authors=6 |vauthors=Tripp HJ, Bench SR, Turk KA, Foster RA, Desany BA, Niazi F, Affourtit JP, Zehr JP |date=March 2010 |title=Metabolic streamlining in an open-ocean nitrogen-fixing cyanobacterium |journal=Nature |volume=464 |issue=7285 |pages=90–94 |bibcode=2010Natur.464...90T |doi=10.1038/nature08786 |pmid=20173737 |s2cid=205219731}}</ref> ''G''enes are lacking for photosystem II of the photosynthetic apparatus, RuBisCO (ribulose-1,5-bisphosphate carboxylase/oxygenase), and enzymes of the Calvin and tricarboxylic acid (TCA) cycle.<ref name="Zehr_2008">{{cite journal | vauthors = Zehr JP, Bench SR, Carter BJ, Hewson I, Niazi F, Shi T, Tripp HJ, Affourtit JP | display-authors = 6 | title = Globally distributed uncultivated oceanic N2-fixing cyanobacteria lack oxygenic photosystem II | journal = Science | volume = 322 | issue = 5904 | pages = 1110–1112 | date = November 2008 | pmid = 19008448 | doi = 10.1126/science.1165340 | bibcode = 2008Sci...322.1110Z | s2cid = 206516012 }}</ref><ref>{{cite journal | vauthors = Bothe H, Tripp HJ, Zehr JP | title = Unicellular cyanobacteria with a new mode of life: the lack of photosynthetic oxygen evolution allows nitrogen fixation to proceed | journal = Archives of Microbiology | volume = 192 | issue = 10 | pages = 783–790 | date = October 2010 | pmid = 20803290 | doi = 10.1007/s00203-010-0621-5 | bibcode = 2010ArMic.192..783B | s2cid = 30256291 }}</ref> Due to the lack of metabolically essential genes, ''A. thalassa'' requires external sources of carbon and other biosynthetic compounds.<ref name="Tripp_2010" /> As well, ''A. thalassa lacks'' the tricarboxylic acid cycle, but expresses a putative dicarboxylic-acid transporter.<ref name="Tripp_2010" /> This suggests that ''A. thalassa'' fills its requirement for dicarboxylic acids from an external source.<ref name="Tripp_2010" /> The complete or partial lack of biosynthetic enzymes required for valine, leucine, isoleucine, phenylalanine, tyrosine and tryptophan biosynthesis further suggests the need for external sources of amino acids.<ref name="Tripp_2010" /> However, ''A. thalassa'' still possesses the Fe-III transport genes (''afuABC''), which should allow for the transport of Fe-III into the cell.<ref name="Zehr_2016">{{cite journal | vauthors = Zehr JP, Shilova IN, Farnelid HM, Muñoz-Marín MC, Turk-Kubo KA | title = Unusual marine unicellular symbiosis with the nitrogen-fixing cyanobacterium UCYN-A | journal = Nature Microbiology | volume = 2 | issue = 1 | article-number = 16214 | date = December 2016 | pmid = 27996008 | doi = 10.1038/nmicrobiol.2016.214 | bibcode = 2016NatMb...216214Z | s2cid = 27516275 | url = https://escholarship.org/uc/item/3jc282mc | access-date = 28 March 2022 | archive-date = 28 March 2022 | archive-url = https://web.archive.org/web/20220328084818/https://escholarship.org/uc/item/3jc282mc | url-status = live | hdl = 10396/29192 | hdl-access = free }}</ref>

=== Obligate symbiosis === ''Atelocyanobacterium thalassa'' is an obligate symbiote of the calcifying haptophyte alga ''Braarudosphaera bigelowii''.<ref name="Thompson_2012" /> Stable isotope experiments revealed that ''A. thalassa'' fixes 15N2 and exchanges fixed nitrogen with the partner, while H13CO3- was fixed by ''B. bigelowii'' and exchanged to ''A. thalassa''. ''A. thalassa'' receives ~16% of the total carbon of the symbiotic partner, and exchanges ~85 -95% of total fixed nitrogen in return.<ref name="Thompson_2012" /><ref name="Krupke_2015">{{cite journal | vauthors = Krupke A, Mohr W, LaRoche J, Fuchs BM, Amann RI, Kuypers MM | title = The effect of nutrients on carbon and nitrogen fixation by the UCYN-A-haptophyte symbiosis | journal = The ISME Journal | volume = 9 | issue = 7 | pages = 1635–1647 | date = July 2015 | pmid = 25535939 | pmc = 4478704 | doi = 10.1038/ismej.2014.253 | bibcode = 2015ISMEJ...9.1635K }}</ref>

''Atelocyanobacterium thalassa'' must live in close physical association with its metabolically dependent symbiosis partner; however, the details of the physical interaction are still unclear due to a lack of clear microscopy images.<ref name="Zehr_2016" /> ''Atelocyanobacterium thalassa'' may be a true endosymbiont and fully enclosed within the host's cell membrane or has molecular mechanisms to allow for secure attachment and transfer of metabolites.<ref name="Krupke_2015" /> This symbiotic connection must not allow the passage of oxygen while maintaining an exchange of fixed nitrogen and carbon.<ref name="Krupke_2015" /> Such close symbiosis also requires signalling pathways between the partners and synchronized growth.<ref name="Krupke_2015" />

A stable co-culture of UCYN-A2 and its host was obtained and subjected to imaging studies. The UCYN-A2 "nitroplast" lineage imports a wide variety proteins from the host, triggered by a unique signal sequence, making it subject to tight control by the host cell. Its light-dark cycle is kept in sync with the host cell by host cryptochrome proteins. Several of its metabolic pathways are only complete with the help of host proteins.<ref name="Coale_2024"/>

=== Daytime N-fixation === ''Atelocyanobacterium thalassa'' is unicellular, hence it does not have specialized cellular compartments (heterocysts) to protect the nitrogenase (''nifH'') from oxygen exposure. Other nitrogen-fixing organisms employ temporal separation by fixing nitrogen only at night-time, however, ''A. thalassa'' has been found to express the ''nifH'' gene during the daylight.<ref name="Church_2005">{{cite journal |vauthors=Church MJ, Short CM, Jenkins BD, Karl DM, Zehr JP |date=September 2005 |title=Temporal patterns of nitrogenase gene (''nifH'') expression in the oligotrophic North Pacific Ocean |journal=Applied and Environmental Microbiology |volume=71 |issue=9 |pages=5362–5370 |bibcode=2005ApEnM..71.5362C |doi=10.1128/aem.71.9.5362-5370.2005 |pmc=1214674 |pmid=16151126}}</ref><ref name="Zehr_2008" /> This is possible due to the absence of photosystem II and, therefore, oxygen and transcriptional control.<ref name="Zehr_2008" /><ref name="Maria del Carmen Muñoz-Marin 2019">{{Cite journal |vauthors = Muñoz-Marín MC, Shilova IN, Shi T, Farnelid H, Cabello AM, Zehr JP |date=January 2019 |title=The transcriptional cycle is suited to daytime N2 fixation in the unicellular cyanobacterium "''Candidatus'' Atelocyanobacterium thalassa" (UCYN-A) |publisher=American Society for Microbiology |journal=mBio |volume=10 |issue=1 |article-number=e02495-18 |doi=10.1128/mBio.02495-18 |doi-access=free |pmc=6315102 |pmid=30602582}}</ref> It is hypothesized that the day-time nitrogen-fixation is more energy-efficient than night-time fixation common in other diazotrophs because light energy can be used directly for the energy-intensive nitrogen fixation.{{r|Maria del Carmen Muñoz-Marin 2019}}

== Life cycle == The lifecycle of ''A. thalassa'' is not well understood. As an obligate endosymbiont, ''A. thalassa'' is thought to be unable to survive outside of the host, suggesting its entire life cycle takes place inside of the host.<ref name="Zehr_2016" /> The division and replication of ''A. thalassa'' are at least partially under the control of the host cell.<ref>{{Cite journal |last1=Landa |first1=Marine |last2=Turk-Kubo |first2=Kendra A. |last3=Cornejo-Castillo |first3=Francisco M. |last4=Henke |first4=Britt A. |last5=Zehr |first5=Jonathan P. |date=5 May 2021 |title=Critical Role of Light in the Growth and Activity of the Marine N2-Fixing UCYN-A Symbiosis |journal=Frontiers in Microbiology |volume=12 |article-number=666739 |doi=10.3389/fmicb.2021.666739 |pmid=34025621 |pmc=8139342 |issn=1664-302X|doi-access=free }}</ref> It is thought that a signal transduction pathway exists to regulate the amount of ''A. thalassa'' cells within the host to ensure a sufficient amount of ''A. thalassa'' cells are supplied to the host's daughter cell during cell division.<ref name="Zehr_2016" />

UCYN-A2's cell division cadence is kept in sync with the host, like the mitochondria and the chloroplasts.<ref name="Coale_2024"/>

== Diversity == Genomic analysis of ''A. thalassa'' shows a wide variety of ''nifH'' gene sequences. Thus, this group of cyanobacteria can be divided into genetically distinct sublineages, four of which have been identified and defined. ''Sequences belonging to A. thalassa'' have been found in nearly all oceanic bodies.<ref name=":0">{{Cite journal |vauthors=Farnelid H, Turk-Kubo K, Muñoz-Marín MC, Zehr JP |date=16 September 2016 |title=New insights into the ecology of the globally significant uncultured nitrogen-fixing symbiont UCYN-A |url=https://www.int-res.com/abstracts/ame/v77/n3/p125-138/ |journal=Aquatic Microbial Ecology |language=en |volume=77 |issue=3 |pages=125–138 |doi=10.3354/ame01794 |issn=0948-3055 |doi-access=free |bibcode=2016AqME...77..125F |access-date=28 March 2022 |archive-date=2 February 2022 |archive-url=https://web.archive.org/web/20220202192147/http://www.int-res.com/abstracts/ame/v77/n3/p125-138/ |url-status=live |hdl=10396/29191 |hdl-access=free }}</ref>

=== Lineages === The lineages of ''A. thalassa'' are split by their determining oligotypes. There is a very high level of similarity between all sublineages in their amino-acid sequences, but some variance was found in their ''nifH'' sequences. The oligotypes of ''A. thalassa'' are based on its nitrogenase (''nifH'') sequences, and reveal thirteen positions of variance (entropy).<ref name="Turk-Kubo_2017" /> The variances would cause different oligotypes/sublineages of ''A. thalassa'' to be found in different relative abundances and have different impacts on the ecosystems where they are found. Four main sublineages have been identified from oligotype analysis, and their respective oligotypes are: UCYN-A1/Oligo1, UCYN-A2/Oligo2, UCYN-A3/Oligo3, UCYN-A4/Oligo4. As many as 8 sublineages have been distinguished.<ref name=Henke18>{{cite journal |last1=Henke |first1=Britt A. |last2=Turk-Kubo |first2=Kendra A. |last3=Bonnet |first3=Sophie |last4=Zehr |first4=Jonathan P. |title=Distributions and Abundances of Sublineages of the N2-Fixing Cyanobacterium ''Candidatus'' Atelocyanobacterium thalassa (UCYN-A) in the New Caledonian Coral Lagoon |journal=Frontiers in Microbiology |date=5 April 2018 |volume=9 |article-number=554 |doi=10.3389/fmicb.2018.00554 |doi-access=free |bibcode=2018FrMic...900554H }}</ref>

UCYN-A1 was the most abundant oligotype found across the oceans.<ref name="Turk-Kubo_2017" /> The UCYN-A1 sublineage has an abundance of nitrogenase in a range of 104 – 107 copies of ''nifH'' per litre.<ref>{{Cite journal | vauthors = Mulholland MR, Bernhardt PW, Blanco-Garcia JL, Mannino A, Hyde K, Mondragon E, Turk K, Moisander PH, Zehr JP | display-authors = 6 |date=24 June 2012 |title=Rates of dinitrogen fixation and the abundance of diazotrophs in North American coastal waters between Cape Hatteras and Georges Bank |journal=Limnology and Oceanography |volume=57 |issue=4 |pages=1067–1083 |doi=10.4319/lo.2012.57.4.1067 |doi-access=free| bibcode = 2012LimOc..57.1067M | hdl = 2060/20140006592 | s2cid = 13692577 |issn=0024-3590|hdl-access=free }}</ref> UCYN-A1 and UCYN-A2 also have a significantly reduced genome size. UCYN-A2 differs from UCYN-A1 in that its oligo2 oligotyping has 10/13 differing positions of entropy from oligo1 (UCYN-A1). They also have different hosts. UCYN-A3 differs from UCYN-A1 with its oligo3 differing from oligo1 with an entropy position difference of 8/13. UCYN-A4 also differs from UCYN-A1 by 8/13 entropy positions in a different set.

{|class=wikitable |+''A. thalassa'' lineages ! Lineage !! Environment !! Hosts !! Other traits !! Genome? |- | UCYN-A1 || Open ocean || Unnamed ''Chrysochromulina'' sp.<ref name=Cornejo19/>{{rp|at=Fig.S7}} (1–3 μm)<ref name="Cornejo16">{{cite journal |last1=Cornejo-Castillo |first1=Francisco M. |last2=Cabello |first2=Ana M. |last3=Salazar |first3=Guillem |last4=Sánchez-Baracaldo |first4=Patricia |last5=Lima-Mendez |first5=Gipsi |last6=Hingamp |first6=Pascal |last7=Alberti |first7=Adriana |last8=Sunagawa |first8=Shinichi |last9=Bork |first9=Peer |last10=de Vargas |first10=Colomban |last11=Raes |first11=Jeroen |last12=Bowler |first12=Chris |last13=Wincker |first13=Patrick |last14=Zehr |first14=Jonathan P. |last15=Gasol |first15=Josep M. |last16=Massana |first16=Ramon |last17=Acinas |first17=Silvia G. |title=Cyanobacterial symbionts diverged in the late Cretaceous towards lineage-specific nitrogen fixation factories in single-celled phytoplankton |journal=Nature Communications |date=22 March 2016 |volume=7 |issue=1 |article-number=11071 |doi=10.1038/ncomms11071 |doi-access=free |bibcode=2016NatCo...711071C }}</ref> || || GCA_000025125.1 (full) |- | UCYN-A2 || Coastal || ''B. bigelowii'' (4–10 μm)<ref name="Cornejo16"/> || Nitroplast || GCA_020885515.1 (full) |- | UCYN-A3 || Open ocean<ref name=Cornejo19>{{cite journal |last1=Cornejo-Castillo |first1=Francisco M. |last2=Muñoz-Marín |first2=María del Carmen |last3=Turk-Kubo |first3=Kendra A. |last4=Royo-Llonch |first4=Marta |last5=Farnelid |first5=Hanna |last6=Acinas |first6=Silvia G. |last7=Zehr |first7=Jonathan P. |title=UCYN-A3, a newly characterized open ocean sublineage of the symbiotic N2-fixing cyanobacterium ''Candidatus'' Atelocyanobacterium thalassa |journal=Environmental Microbiology |date=January 2019 |volume=21 |issue=1 |pages=111–124 |doi=10.1111/1462-2920.14429|pmid=30255541 |bibcode=2019EnvMi..21..111C |hdl=10396/29195 |url=https://escholarship.org/content/qt4s3426q3/qt4s3426q3.pdf}}</ref> || ''B. bigelowii'' || || Unpublished (~13%) |- | UCYN-A4 || Coastal || ''B. bigelowii'' genotype I<ref name=Kantor24>{{cite journal |last1=Kantor |first1=EJH |last2=Robicheau |first2=BM |last3=Tolman |first3=J |last4=Archibald |first4=JM |last5=LaRoche |first5=J |title=Metagenomics reveals the genetic diversity between sublineages of UCYN-A and their algal host plastids. |journal=ISME Communications |date=January 2024 |volume=4 |issue=1 |article-number=ycae150 |doi=10.1093/ismeco/ycae150 |doi-access=free |pmid=39670058 |pmc=11637426}}</ref> || Nitroplast-like (possibly more derived than A2)<ref name=Kantor24/> || GCA_051971635.1 (near-full) |}

Oligotypes are used because ''nifH'' is more easily detected in an intact form environmental samples compared to full metagenomes that require a larger amount of samples as well as sequencing work. Where available, however, full genomes are able to show more information. Complete genomes of the A1 and A2 sublineages, combined with a molecular clock approach, show that the two lineages diverged in the late Cretaceous (~90 million years ago), corroborated by fossil records of ''B. bigelowii'' going back about 100 million years. These lineages have likely co-evolved with their hosts.<ref name="Cornejo16"/>

As of GTDB Release 10-RS226 (April 2025), the NCBI GenBank contains 8 ''A. thalassa'' genomes of sufficient quality and completeness for analysis. GTDB assigns UCYN-A1 (GCA_000025125.1 + 5 others) and UCYN-A2 (GCA_020885515.1 + 1 other) to two separate species-level clusters.<ref>{{cite web |title=GTDB - Tree at g__Atelocyanobacterium |url=https://gtdb.ecogenomic.org/tree?r=g__Atelocyanobacterium |website=gtdb.ecogenomic.org}}</ref>

=== Phylogeny === Cornejo-Castillo ''et al'', 2019. ''nifH'', maximum likelihood. Taxonomy corrected per NCBI and GTDB where applicable.<ref name=Cornejo19/>

{{clade |style=font-size:85%;line-height:85%; |1={{clade |1={{clade |1={{clade|UCYN-A1|UCYN-A2}} |2=UCYN-A3}} |2=UCYN-A4 }} |2={{clade|1=''Gloeothece'' sp. K068DGA|2={{clade|endosymbiont of ''Rhopalodia gibba'' (see ''Epithemia'' § Endosymbiosis, under GTDB genus ''Rippkaea'')|{{clade|''Crocosphaera chwakensis'' CCY0110|''Crocosphaera subtropica'' ATCC 51142}}}}}} |3={{clade |1={{clade|''Rippkaea orientalis'' PCC 8001, PCC 8002|''Synechococcus'' sp. RF-1}} |2={{clade |1={{clade|''Gloeothece verrucosa'' PCC 7822 |''Gloeothece citriformis'' PCC 7424}} |2={{clade |1={{clade|''Lyngbya aestuarii'' PCC 8106|''Lyngbya majuscula'' CCAP 1446/4}} |2=''Crocosphaera watsonii'' WH 8501, WH 0003}}}}}} }}

Cornejo-Castillo ''et al'', 2019. Phylogenomic (165 protein-coding sequences), maximum likelihood. Taxonomy corrected per NCBI and GTDB where applicable.<ref name=Cornejo19/>{{rp|at=Fig.S6}}

{{clade | style=font-size:85%;line-height:85%; |2=''Pleurocapsa'' sp. PCC 7327 |1={{clade |1={{clade|''Gloeothece verrucosa'' PCC 7822 |''Gloeothece citriformis'' PCC 7424}} |2={{clade |1={{clade|''Rippkaea orientalis'' PCC 8001, PCC 8002|endosymbiont of ''Rhopalodia gibba''}} |2={{clade |1=''Crocosphaera subtropica'' ATCC 51142 |2={{clade|1=UCYN-A1|2={{clade|UCYN-A2|UCYN-A3}}}}}}}}}} }}

The phylogenomic result is considered more representative of the life-history of organisms than the single-locus ''nifH'' result.<ref name=Cornejo19/>

== Genome evolution == As other endosymbiotic organelles, nitroplast genome lost many genes and many essential biosynthetic pathways of them should be supported by the proteins produced in the nucleus.

After analyzing the genome and proteome in the nitroplast, scientists found that three types of proteins coexist in nitoplast, UCYN-1 encoded proteins, ''B. bigelowii'' encoded proteins (nucleus encoded), and the proteins encoded by both ("redundancies").

Each ''B. bigelowii'' encoded protein contains a special sequence named uTP (UCYN transition peptide), an extension at {{prime|3}} end of functional regions, which make them much longer than orthologous proteins found in other species. The uTP sequences assist the transition of proteins from nucleus to nitroplast. Actually, some ''B. bigelowii'' encoded proteins were not detected in nitroplast, but the existence of uTP sequence suggested that they might be transported into nitroplast.

Some proteins, like PyrC in the pyrimidine biosynthesis pathway, are produced in both nucleus and nitroplast. The scientists said that such redundancies might be the key reason why UCYN-1 lost genes faster than chromatophore in ''Paulinella'', whose endosymbiosis event happened in similar time.<ref name="Coale_2024"/>

== Implications == The discovery of nitroplasts challenges previous notions about the exclusivity of nitrogen fixation to prokaryotic organisms. Understanding the structure and function of nitroplasts opens up possibilities for genetic engineering in plants.<ref name="nature.com"/> By incorporating genes responsible for nitroplast function, researchers aim to develop crops capable of fixing their own nitrogen, potentially reducing the need for nitrogen-based fertilizers and mitigating environmental damage.<ref name="nature.com"/>

== References == {{notelist}} {{Reflist|30em}}

== Further reading == *{{Cite journal |last=Massana |first=Ramon |date=2024-04-12 |title=The nitroplast: A nitrogen-fixing organelle |url=https://www.science.org/doi/10.1126/science.ado8571 |journal=Science |language=en |volume=384 |issue=6692 |pages=160–161 |doi=10.1126/science.ado8571 |pmid=38603513 |bibcode=2024Sci...384..160M |issn=0036-8075|hdl=10261/354070 |hdl-access=free |url-access=subscription }} * {{cite web |last=Baisas |first=Laura |title=For the first time in one billion years, two lifeforms truly merged into one organism |website=Popular Science |date=2024-04-18 |url=https://www.popsci.com/science/two-lifeforms-merged-into-one/ |access-date=2024-04-19}}

== External links == * [http://www.expasy.org/sprot/hamap/UCYNA.html HAMAP: cyanobacterium UCYN-A complete proteome] * [http://www.astrobio.net/pressrelease/3412/life-stripped-down Life Stripped Down] * [http://www.futura-sciences.com/fr/news/t/biologie-3/d/ucyn-a-la-cyanobacterie-qui-fixe-lazote-mais-ignore-la-photosynthese_17366-1/ UCYN-A, la cyanobactérie qui fixe l'azote mais ignore la photosynthèse] {{Webarchive|url=https://web.archive.org/web/20100701124014/http://www.futura-sciences.com/fr/news/t/biologie-3/d/ucyn-a-la-cyanobacterie-qui-fixe-lazote-mais-ignore-la-photosynthese_17366-1/ |date=1 July 2010 }} French journal article about UCYN-A * [https://www.science.org/doi/abs/10.1126/science.1165340 Globally Distributed Uncultivated Oceanic N2-Fixing Cyanobacteria Lack Oxygenic Photosystem II]

Category:Environmental microbiology Category:Chroococcales Category:Candidatus taxa Category:Marine microorganisms Category:Algal anatomy Category:Organelles Category:Endosymbiotic events