Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean

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dc.contributor.authorAylward, Frank O.en
dc.contributor.authorSantoro, Alyson E.en
dc.contributor.departmentBiological Sciencesen
dc.date.accessioned2021-09-23T12:46:27Zen
dc.date.available2021-09-23T12:46:27Zen
dc.date.issued2020-05-01en
dc.date.updated2021-09-23T12:46:23Zen
dc.description.abstractThe Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of ∼1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations. Importance: It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.en
dc.description.versionPublished versionen
dc.format.extent20 page(s)en
dc.format.mimetypeapplication/pdfen
dc.identifierARTN e00415-20 (Article number)en
dc.identifier.doihttps://doi.org/10.1128/mSystems.00415-20en
dc.identifier.eissn2379-5077en
dc.identifier.issn2379-5077en
dc.identifier.issue3en
dc.identifier.orcidAylward, Frank [0000-0002-1279-4050]en
dc.identifier.other5/3/e00415-20 (PII)en
dc.identifier.pmid32546674en
dc.identifier.urihttp://hdl.handle.net/10919/105046en
dc.identifier.volume5en
dc.language.isoenen
dc.publisherAmerican Society for Microbiologyen
dc.relation.urihttp://gateway.webofknowledge.com/gateway/Gateway.cgi?GWVersion=2&SrcApp=PARTNER_APP&SrcAuth=LinksAMR&KeyUT=WOS:000576704600022&DestLinkType=FullRecord&DestApp=ALL_WOS&UsrCustomerID=930d57c9ac61a043676db62af60056c1en
dc.rightsCreative Commons Attribution 4.0 Internationalen
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/en
dc.subjectLife Sciences & Biomedicineen
dc.subjectMicrobiologyen
dc.subjectThaumarchaeotaen
dc.subjectmarine archaeaen
dc.subjectTACKen
dc.subjectPQQ-dehydrogenaseen
dc.subjectRuBisCOen
dc.subjectQUINOPROTEIN GLUCOSE-DEHYDROGENASEen
dc.subjectALCOHOL-DEHYDROGENASEen
dc.subjectCRYSTAL-STRUCTUREen
dc.subjectESCHERICHIA-COLIen
dc.subjectARCHAEAen
dc.subjectEVOLUTIONen
dc.subjectDIVERSITYen
dc.subjectINSIGHTSen
dc.subjectDATABASEen
dc.subjectTREEen
dc.titleHeterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Oceanen
dc.title.serialmSystemsen
dc.typeArticle - Refereeden
dc.type.dcmitypeTexten
dc.type.otherArticleen
dc.type.otherJournalen
pubs.organisational-group/Virginia Techen
pubs.organisational-group/Virginia Tech/Scienceen
pubs.organisational-group/Virginia Tech/Science/Biological Sciencesen
pubs.organisational-group/Virginia Tech/Faculty of Health Sciencesen
pubs.organisational-group/Virginia Tech/All T&R Facultyen
pubs.organisational-group/Virginia Tech/Science/COS T&R Facultyen

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