A widespread porin-cytochrome complex Om(abc)B kickstarts microbial respiration and nanowire formation

A widespread porin-cytochrome complex Om(abc)B kickstarts microbial respiration and nanowire formation | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article A widespread porin-cytochrome complex Om(abc)B kickstarts microbial respiration and nanowire formation Joseph Erwin, Cong Shen, Vanessa Saldivar, Aldo Salazar Morales, and 6 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5369439/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Microbial respiration via extracellular electron transfer (EET) drives several globally-important environmental processes and has applications in bioenergy, bioremediation, and bioelectronics. Geobacter sulfurreducens produce micrometer-long cytochrome nanowires for long-range (>10 µm) EET, but also require transmembrane porin-cytochrome complexes (PCCs), which can only perform EET on the cell surface. It was unknown why cells performing long-range EET need both PCCs and nanowires. Using Om(abc)B and OmcS as a model PCC and nanowire, respectively, for EET to Fe(III), we show that PCCs and nanowires form sequential, independent EET pathways where PCCs first kickstart EET and provide energy crucial for nanowire synthesis, and then nanowires perform long-range EET. Our model explains why both PCCs and nanowires are necessary. To understand the underlying EET mechanism, we purified native Om(ab)B and OmcB and found high excitonic coupling among hemes. Their midpoint reduction potentials (-182, -167 mV, respectively) are tuned for efficient electron transport. Additionally, OmcB transfers electrons to Fe(III) ~5 times more efficiently than OmcS. Our work suggests that the metabolic trade-off between PCCs and nanowires results from efficient proteome allocation. Notably, PCCs are widespread in environmentally-important bacteria and co-evolved with OmcS nanowires. This previously-undescribed nanowire synthesis strategy could accelerate EET in diverse microbes and environments. Biological sciences/Microbiology/Environmental microbiology/Soil microbiology Earth and environmental sciences/Biogeochemistry/Element cycles Physical sciences/Chemistry/Electrochemistry/Fuel cells Physical sciences/Chemistry/Biochemistry/Bioinorganic chemistry/Metalloproteins Biological sciences/Biophysics/Bioenergetics Full Text Additional Declarations There is NO Competing Interest. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5369439","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":377872133,"identity":"760a4f39-98f2-47e9-922c-878a86c5f033","order_by":0,"name":"Joseph Erwin","email":"","orcid":"","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Joseph","middleName":"","lastName":"Erwin","suffix":""},{"id":377872134,"identity":"4b24e0de-72dc-4399-929c-d86aec18e3bc","order_by":1,"name":"Cong Shen","email":"","orcid":"https://orcid.org/0000-0003-3468-5629","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Cong","middleName":"","lastName":"Shen","suffix":""},{"id":377872135,"identity":"cf274417-3c6d-452c-8a26-2774830c3b13","order_by":2,"name":"Vanessa Saldivar","email":"","orcid":"","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Vanessa","middleName":"","lastName":"Saldivar","suffix":""},{"id":377872136,"identity":"0e04b043-7166-422c-9529-57eb628cf3ad","order_by":3,"name":"Aldo Salazar Morales","email":"","orcid":"https://orcid.org/0000-0002-8126-9460","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Aldo","middleName":"Salazar","lastName":"Morales","suffix":""},{"id":377872137,"identity":"30d70dec-4ade-42fb-94c4-066cf7b07e25","order_by":4,"name":"Vasilije Pentalic","email":"","orcid":"","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Vasilije","middleName":"","lastName":"Pentalic","suffix":""},{"id":377872138,"identity":"30d94616-60fe-41cd-a6f6-fcbd161a1e70","order_by":5,"name":"Fadel Samatey","email":"","orcid":"","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Fadel","middleName":"","lastName":"Samatey","suffix":""},{"id":377872139,"identity":"5e74ef6f-3a18-4c50-b2f5-32865ec75c5a","order_by":6,"name":"Peter Dahl","email":"","orcid":"","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Peter","middleName":"","lastName":"Dahl","suffix":""},{"id":377872140,"identity":"3a0091ad-1de4-45db-a35d-866b37543498","order_by":7,"name":"Yangqi Gu","email":"","orcid":"https://orcid.org/0000-0002-8206-8804","institution":"Medical Research Council Laboratory of Molecular Biology","correspondingAuthor":false,"prefix":"","firstName":"Yangqi","middleName":"","lastName":"Gu","suffix":""},{"id":377872141,"identity":"f0e284d7-9654-46c6-abeb-c0e0f0059dfc","order_by":8,"name":"Sibel Ebru Yalcin","email":"","orcid":"https://orcid.org/0000-0002-6041-5297","institution":"Yale University","correspondingAuthor":false,"prefix":"","firstName":"Sibel","middleName":"Ebru","lastName":"Yalcin","suffix":""},{"id":377872132,"identity":"cd383cbc-5099-406c-992f-78aa170b9bab","order_by":9,"name":"Nikhil Malvankar","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABEUlEQVRIie3RMUvDQBTA8VcCl+UgjldCv8OTQKVY+kVcIoF0MZix4NBIQBdxjot+hXZxTnmQLAHXA5d8AIeAS0FBL22HDubqKHj/5d4Nv+O4AzCZ/mIWY+DHarDbXQ7gAPTUAr1ES7AddqSfbBYNAUVgn2B+gJzYLKxrhDMn5cfvcTW59GRQ5w2MB4v8ZzJKWYnqYlFG3HMzGYyeZYirDEKviyDZN6IlCTHf5Y2FQ+kjcaDzg+SJWPDBmzl62bShT/jSEFZsyIKswuWSEMUFknoBHQkVEdFSkVNelSiqt3h1h4H30EVeimF/PRtHj+V1+sqLK3Rup8t6PZsM7jvILrE3H/mw/anf5+hPN5lMpv/XNxm1Yd0gFQ9AAAAAAElFTkSuQmCC","orcid":"https://orcid.org/0000-0001-5611-6633","institution":"Yale University","correspondingAuthor":true,"prefix":"","firstName":"Nikhil","middleName":"","lastName":"Malvankar","suffix":""}],"badges":[],"createdAt":"2024-10-31 22:55:07","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5369439/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5369439/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":69935061,"identity":"d9088f44-b774-4627-bef0-5ed0e7b68d94","added_by":"auto","created_at":"2024-11-26 18:49:53","extension":"pdf","order_by":1,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":2917319,"visible":true,"origin":"","legend":"","description":"","filename":"2.Malvankarmanuscriptlinenumbers.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5369439/v1_covered_31317de1-e24a-4686-a4a5-f9981e53d675.pdf"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e Competing Interest.","formattedTitle":"A widespread porin-cytochrome complex Om(abc)B kickstarts microbial respiration and nanowire formation","fulltext":[],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":false,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":true,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":true,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":true,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"","lastPublishedDoi":"10.21203/rs.3.rs-5369439/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-5369439/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"Microbial respiration via extracellular electron transfer (EET) drives several globally-important environmental processes and has applications in bioenergy, bioremediation, and bioelectronics. \u003ci\u003eGeobacter sulfurreducens\u003c/i\u003e produce micrometer-long cytochrome nanowires for long-range (\u003e10 µm) EET, but also require transmembrane porin-cytochrome complexes (PCCs), which can only perform EET on the cell surface. It was unknown why cells performing long-range EET need both PCCs and nanowires. Using Om(abc)B and OmcS as a model PCC and nanowire, respectively, for EET to Fe(III), we show that PCCs and nanowires form sequential, independent EET pathways where PCCs first kickstart EET and provide energy crucial for nanowire synthesis, and then nanowires perform long-range EET. Our model explains why both PCCs and nanowires are necessary. To understand the underlying EET mechanism, we purified native Om(ab)B and OmcB and found high excitonic coupling among hemes. Their midpoint reduction potentials (-182, -167 mV, respectively) are tuned for efficient electron transport. Additionally, OmcB transfers electrons to Fe(III) ~5 times more efficiently than OmcS. Our work suggests that the metabolic trade-off between PCCs and nanowires results from efficient proteome allocation. Notably, PCCs are widespread in environmentally-important bacteria and co-evolved with OmcS nanowires. This previously-undescribed nanowire synthesis strategy could accelerate EET in diverse microbes and environments.","manuscriptTitle":"A widespread porin-cytochrome complex Om(abc)B kickstarts microbial respiration and nanowire formation","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-11-21 13:07:20","doi":"10.21203/rs.3.rs-5369439/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"25ff733e-e55a-42ea-ad66-054014f91453","owner":[],"postedDate":"November 21st, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[{"id":40235683,"name":"Biological sciences/Microbiology/Environmental microbiology/Soil microbiology"},{"id":40235684,"name":"Earth and environmental sciences/Biogeochemistry/Element cycles"},{"id":40235685,"name":"Physical sciences/Chemistry/Electrochemistry/Fuel cells"},{"id":40235686,"name":"Physical sciences/Chemistry/Biochemistry/Bioinorganic chemistry/Metalloproteins"},{"id":40235687,"name":"Biological sciences/Biophysics/Bioenergetics"}],"tags":[],"updatedAt":"2024-11-26T18:42:19+00:00","versionOfRecord":[],"versionCreatedAt":"2024-11-21 13:07:20","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5369439","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5369439","identity":"rs-5369439","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}