August 6, 2019 u vol. 116 u no. 32

From the Cover

15973 Cyanobacterial symbionts and cryptic lineage 15861 Neural response to facial emotion 15979 Bacterial interactions and toxic environments 16012 Nunavik Inuit genetic history 16028 Mitochondrial DNA and nuclear epigenome

Contents

THIS WEEK IN PNAS

Cover image: Pictured is a differential 15747 In This Issue interference contrast micrograph of marine dinoflagellate Ornithocercus INNER WORKINGS—An over-the-shoulder look at scientists at work thumii with cyanobacterial symbionts. 15749 How diamonds embedded in meteorites could offer a glimpse into the mantle Takuro Nakayama et al. sequenced the of Mars genome of the cyanobacterium OmCyn, Nola Taylor Redd which is symbiotically associated with single-celled dinoflagellates, and found QNAS that the bacteria represent an underdescribed lineage within an 15752 QnAs with David Reich ecologically important group. Although Beth Azar OmCyn are distributed throughout the world’s oceans, they exist only with PROFILE dinoflagellate hosts, suggesting that there may be other undiscovered cryptic 15754 Profile of Rodolphe Barrangou cyanobacterial lineages. See the article Tinsley H. Davis by Nakayama et al. on pages 15973– See Inaugural Article on page 15774 15978. Image courtesy of Takuro Nakayama. COMMENTARIES 15757 Genomics reveals alga-associated cyanobacteria hiding in plain sight John M. Archibald See companion article on page 15973 15760 Refining the stress gradient hypothesis in a microbial community Sarah P. Hammarlund and William R. Harcombe See companion article on page 15979 15763 Mitochondrial genetics regulate nuclear gene expression through metabolites Jessica L. Fetterman and Scott W. Ballinger See companion article on page 16028

LETTERS 15766 Availability of public databases for triangulation of findings Matthew Lyon, Marcus Munafo, Tom Gaunt, and George Davey Smith 15768 Reply to Lyon et al.: Self-regulation and the foraging gene: From flies to humans Marla B. Sokolowski, Abigail A. Scholer, and James Danckert 15770 The buffering capacity of the brain and optic nerve against spaceflight-associated neuro-ocular syndrome Peter Wostyn, Thomas H. Mader, Charles Robert Gibson, and Peter Paul De Deyn

Free online through the PNAS open access option. PNAS u August 6, 2019 u vol. 116 u no. 32 u iii–vi Downloaded by guest on September 29, 2021 15772 Reply to Wostyn et al.: Investigating the 15830 Membraneless polyester microdroplets as primordial spaceflight-associated neuro-ocular syndrome compartments at the origins of life and the human brain in lockstep Tony Z. Jia, Kuhan Chandru, Yayoi Hongo, Rehana Afrin, Angelique Van Ombergen, Steven Jillings, Elena Tomohiro Usui, Kunihiro Myojo, and H. James Cleaves II Tomilovskaya, Floris L. Wuyts, and Peter zu Eulenburg 15836 Exposing the inadequacy of redox formalisms by resolving redox inequivalence within INAUGURAL ARTICLE isovalent clusters Amymarie K. Bartholomew, Justin J. Teesdale, Rau´l Herna´ndez 15774 Genome editing using the endogenous type I Sa´nchez, Brian J. Malbrecht, Cristin E. Juda, Gabriel Me´nard, CRISPR-Cas system in Lactobacillus crispatus Wei Bu, Diana A. Iovan, Alexandre A. Mikhailine, Shao-Liang Claudio Hidalgo-Cantabrana, Yong Jun Goh, Meichen Pan, Zheng, Ritimukta Sarangi, SuYin Grass Wang, Yu-Sheng Chen, Rosemary Sanozky-Dawes, and Rodolphe Barrangou and Theodore A. Betley See Profile on page 15754 15924 Insights into the origin of the high energy-conversion efficiency of F1-ATPase Kwangho Nam and Martin Karplus PHYSICAL SCIENCES ENGINEERING APPLIED PHYSICAL SCIENCES 15842 Label-free chemical imaging flow cytometry by 15784 A stepwise mechanism for aqueous two-phase high-speed multicolor stimulated Raman scattering system formation in concentrated antibody solutions Yuta Suzuki, Koya Kobayashi, Yoshifumi Wakisaka, Dinghuan Bradley A. Rogers, Kelvin B. Rembert, Matthew F. Poyton, Deng, Shunji Tanaka, Chun-Jung Huang, Cheng Lei, Chia-Wei Halil I. Okur, Amanda R. Kale, Tinglu Yang, Jifeng Zhang, Sun, Hanqin Liu, Yasuhiro Fujiwaki, Sangwook Lee, Akihiro and Paul S. Cremer Isozaki, Yusuke Kasai, Takeshi Hayakawa, Shinya Sakuma, 15792 Conformational switching of chiral colloidal rafts Fumihito Arai, Kenichi Koizumi, Hiroshi Tezuka, Mary Inaba, Kei regulates raft–raft attractions and repulsions Hiraki, Takuro Ito, Misa Hase, Satoshi Matsusaka, Kiyotaka Joia M. Miller, Chaitanya Joshi, Prerna Sharma, Arvind Shiba, Kanako Suga, Masako Nishikawa, Masahiro Jona, Baskaran, Aparna Baskaran, Gregory M. Grason, Michael F. Yutaka Yatomi, Yaxiaer Yalikun, Yo Tanaka, Takeaki Sugimura, Hagan, and Zvonimir Dogic Nao Nitta, Keisuke Goda, and Yasuyuki Ozeki

BIOPHYSICS AND COMPUTATIONAL BIOLOGY STATISTICS 15895 Perturbation of the interactions of calmodulin with 15849 Reconciling modern machine-learning practice GRK5 using a natural product chemical probe and the classical bias–variance trade-off Tyler S. Beyett, Amy E. Fraley, Emily Labudde, Dhabaleswar Mikhail Belkin, Daniel Hsu, Siyuan Ma, and Soumik Mandal Patra, Ryan C. Coleman, Akito Eguchi, Alisa Glukhova, Qiuyan Chen, Robert M. Williams, Walter J. Koch, David H. Sherman, and John J. G. Tesmer SOCIAL SCIENCES

15930 Assembling multidomain protein structures through PSYCHOLOGICAL AND COGNITIVE SCIENCES analogous global structural alignments 15855 Developmental topography of cortical thickness Xiaogen Zhou, Jun Hu, Chengxin Zhang, Guijun Zhang, during infancy and Yang Zhang Fan Wang, Chunfeng Lian, Zhengwang Wu, Han Zhang, Tengfei Li, Yu Meng, Li Wang, Weili Lin, Dinggang Shen, CHEMISTRY and Gang Li 15802 The final steps of [FeFe]-hydrogenase maturation 15861 The neural representation of facial-emotion Oliver Lampret, Julian Esselborn, Rieke Haas, Andreas Rutz, categories reflects conceptual structure Rosalind L. Booth, Leonie Kertess, Florian Wittkamp, Clare F. Megarity, Fraser A. Armstrong, Martin Winkler, Jeffrey A. Brooks, Junichi Chikazoe, Norihiro Sadato, and Thomas Happe and Jonathan B. Freeman 15811 Mapping hole hopping escape routes in proteins 15871 Credit assignment to state-independent task Ruijie D. Teo, Ruobing Wang, Elizabeth R. Smithwick, Agostino representations and its relationship with Migliore, Michael J. Therien, and David N. Beratan model-based decision making Nitzan Shahar, Rani Moran, Tobias U. Hauser, Rogier A. Kievit, 15817 A photostable fluorescent marker for the Daniel McNamee, Michael Moutoussis, NSPN Consortium, superresolution live imaging of the dynamic and Raymond J. Dolan structure of the mitochondrial cristae Chenguang Wang, Masayasu Taki, Yoshikatsu Sato, Yasushi 15877 Officer characteristics and racial disparities in fatal Tamura, Hideyuki Yaginuma, Yasushi Okada, officer-involved shootings and Shigehiro Yamaguchi David J. Johnson, Trevor Tress, Nicole Burkel, Carley Taylor, and Joseph Cesario 15823 Drugging an undruggable pocket on KRAS Dirk Kessler, Michael Gmachl, Andreas Mantoulidis, Laetitia J. 16056 Prestimulus feedback connectivity biases the content Martin, Andreas Zoephel, Moriz Mayer, Andreas Gollner, David of visual experiences Covini, Silke Fischer, Thomas Gerstberger, Teresa Gmaschitz, Elie Rassi, Andreas Wutz, Nadia Mu¨ller-Voggel, Craig Goodwin, Peter Greb, Daniela Ha¨ring, Wolfgang Hela, and Nathan Weisz Johann Hoffmann, Jale Karolyi-Oezguer, Petr Knesl, Stefan Kornigg, Manfred Koegl, Roland Kousek, Lyne Lamarre, SOCIAL SCIENCES Franziska Moser, Silvia Munico-Martinez, Christoph Peinsipp, Jason Phan, Jo¨rg Rinnenthal, Jiqing Sai, Christian Salamon, 15883 Effects of policy-driven hypothetical air pollutant Yvonne Scherbantin, Katharina Schipany, Renate Schnitzer, interventions on childhood asthma incidence in Andreas Schrenk, Bernadette Sharps, Gabriella Siszler, Qi Sun, southern California Alex Waterson, Bernhard Wolkerstorfer, Markus Zeeb, Mark Erika Garcia, Robert Urman, Kiros Berhane, Rob McConnell, Pearson, Stephen W. Fesik, and Darryl B. McConnell and Frank Gilliland

iv u www.pnas.org Contents Downloaded by guest on September 29, 2021 BIOLOGICAL SCIENCES 15823 Drugging an undruggable pocket on KRAS Dirk Kessler, Michael Gmachl, Andreas Mantoulidis, Laetitia J. Martin, Andreas Zoephel, Moriz Mayer, Andreas Gollner, David APPLIED BIOLOGICAL SCIENCES Covini, Silke Fischer, Thomas Gerstberger, Teresa Gmaschitz, 15889 A tumor-targeted immune checkpoint blocker Craig Goodwin, Peter Greb, Daniela Ha¨ring, Wolfgang Hela, Yuhan Zhang, Changming Fang, Rongsheng E. Wang, Johann Hoffmann, Jale Karolyi-Oezguer, Petr Knesl, Stefan Ying Wang, Hui Guo, Chao Guo, Lijun Zhao, Shuhong Li, Xia Li, Kornigg, Manfred Koegl, Roland Kousek, Lyne Lamarre, Peter G. Schultz, Yu J. Cao, and Feng Wang Franziska Moser, Silvia Munico-Martinez, Christoph Peinsipp, Jason Phan, Jo¨rg Rinnenthal, Jiqing Sai, Christian Salamon, BIOCHEMISTRY Yvonne Scherbantin, Katharina Schipany, Renate Schnitzer, 15802 The final steps of [FeFe]-hydrogenase maturation Andreas Schrenk, Bernadette Sharps, Gabriella Siszler, Qi Sun, Oliver Lampret, Julian Esselborn, Rieke Haas, Andreas Rutz, Alex Waterson, Bernhard Wolkerstorfer, Markus Zeeb, Mark Rosalind L. Booth, Leonie Kertess, Florian Wittkamp, Clare F. Pearson, Stephen W. Fesik, and Darryl B. McConnell Megarity, Fraser A. Armstrong, Martin Winkler, 15967 OsMTOPVIB is required for meiotic bipolar and Thomas Happe spindle assembly 15895 Perturbation of the interactions of calmodulin with Zhihui Xue, Changzhen Liu, Wenqing Shi, Yongjie Miao, Yi GRK5 using a natural product chemical probe Shen, Ding Tang, Yafei Li, Aiqing You, Yunyuan Xu, Kang Tyler S. Beyett, Amy E. Fraley, Emily Labudde, Dhabaleswar Chong, and Zhukuan Cheng Patra, Ryan C. Coleman, Akito Eguchi, Alisa Glukhova, Qiuyan Chen, Robert M. Williams, Walter J. Koch, David H. Sherman, ECOLOGY and John J. G. Tesmer 15973 Single-cell genomics unveiled a cryptic cyanobacterial 15901 The ribosomal protein S1-dependent standby site in lineage with a worldwide distribution hidden by tisB mRNA consists of a single-stranded region a dinoflagellate host and a 5′ structure element Takuro Nakayama, Mami Nomura, Yoshihito Takano, Goro Ce´dric Romilly, Sebastian Deindl, and E. Gerhart H. Wagner Tanifuji, Kogiku Shiba, Kazuo Inaba, Yuji Inagaki, 15907 An essential bifunctional enzyme in Mycobacterium and Masakado Kawata tuberculosis for itaconate dissimilation and See Commentary on page 15757 leucine catabolism 15979 Toxicity drives facilitation between 4 Hua Wang, Alexander A. Fedorov, Elena V. Fedorov, Debbie M. bacterial species Hunt, Angela Rodgers, Holly L. Douglas, Acely Garza-Garcia, Jeffrey B. Philippe Piccardi, Bjo¨rn Vessman, and Sara Mitri Bonanno, Steven C. Almo, and Luiz Pedro So´rio de Carvalho See Commentary on page 15760 15914 Gid10 as an alternative N-recognin of the 15985 Rebuilding global fisheries under uncertainty Pro/N-degron pathway Milad Memarzadeh, Gregory L. Britten, Boris Worm, Artem Melnykov, Shun-Jia Chen, and Alexander Varshavsky and Carl Boettiger BIOPHYSICS AND COMPUTATIONAL BIOLOGY 15991 Plant defenses interact with insect enteric 15811 Mapping hole hopping escape routes in proteins bacteria by initiating a leaky Ruijie D. Teo, Ruobing Wang, Elizabeth R. Smithwick, Agostino gut syndrome Migliore, Michael J. Therien, and David N. Beratan Charles J. Mason, Swayamjit Ray, Ikkei Shikano, Michelle Peiffer, Asher G. Jones, Dawn S. Luthe, Kelli Hoover, 15924 Insights into the origin of the high energy-conversion and Gary W. Felton efficiency of F -ATPase 1 15997 Collective sinking promotes selective cell pairing in Kwangho Nam and Martin Karplus planktonic pennate diatoms 15930 Assembling multidomain protein structures through Joan S. Font-Mun˜oz, Raphae¨l Jeanneret, Jorge Arrieta, analogous global structural alignments Sı´lvia Angle`s, Antoni Jordi, Idan Tuval, Xiaogen Zhou, Jun Hu, Chengxin Zhang, Guijun Zhang, and Gotzon Basterretxea and Yang Zhang 15939 Investigation of the allosteric coupling mechanism in EVOLUTION a glutamate transporter homolog via unnatural 16003 Trading amino acids at the aphid–Buchnera amino acid mutagenesis symbiotic interface Erika A. Riederer and Francis I. Valiyaveetil Honglin Feng, Noel Edwards, Catriona M. H. Anderson, 15947 The allosteric mechanism of substrate-specific transport Mike Althaus, Rebecca P. Duncan, Yu-Ching Hsu, Charles W. in SLC6 is mediated by a volumetric sensor Luetje, Daniel R. G. Price, Alex C. C. Wilson, and David T. Thwaites Michael V. LeVine, Daniel S. Terry, George Khelashvili, Zarek S. Siegel, Matthias Quick, Jonathan A. Javitch, Scott C. Blanchard, and Harel Weinstein GENETICS 15957 Identification of evolutionary and kinetic drivers of 16012 Genetic architecture and adaptations of NAD-dependent signaling Nunavik Inuit Mathias Bockwoldt, Dorothe´e Houry, Marc Niere, Toni I. Sirui Zhou, Pingxing Xie (谢萍星), Ame´lie Quoibion, Gossmann, Ines Reinartz, Alexander Schug, Mathias Ziegler, Amirthagowri Ambalavanan, Alexandre Dionne-Laporte, Dan and Ines Heiland Spiegelman, Cynthia V. Bourassa, Lan Xiong, Patrick A. Dion, and Guy A. Rouleau CELL BIOLOGY 16018 Patronus is the elusive plant securin, 15817 A photostable fluorescent marker for the preventing chromosome separation by superresolution live imaging of the dynamic antagonizing separase structure of the mitochondrial cristae Laurence Cromer, Sylvie Jolivet, Dipesh Kumar Singh, Floriane Chenguang Wang, Masayasu Taki, Yoshikatsu Sato, Yasushi Berthier, Nancy De Winne, Geert De Jaeger, Shinichiro Tamura, Hideyuki Yaginuma, Yasushi Okada, Komaki, Maria Ada Prusicki, Arp Schnittger, Raphael Gue´rois, and Shigehiro Yamaguchi and Raphael Mercier

Contents PNAS u August 6, 2019 u vol. 116 u no. 32 u v Downloaded by guest on September 29, 2021 16028 Regulation of nuclear epigenome by mitochondrial 16080 The neural circuit linking mushroom body parallel DNA heteroplasmy circuits induces memory consolidation in Drosophila Piotr K. Kopinski, Kevin A. Janssen, Patrick M. Schaefer, Sophie Hiroko Awata, Mai Takakura, Yoko Kimura, Ikuko Iwata, Trefely, Caroline E. Perry, Prasanth Potluri, Jesus A. Tomoko Masuda, and Yukinori Hirano Tintos-Hernandez, Larry N. Singh, Kelly R. Karch, Sydney L. 16086 Exosomes regulate neurogenesis and Campbell, Mary T. Doan, Helen Jiang, Itzhak Nissim, Eiko Nakamaru-Ogiso, Kathryn E. Wellen, Nathaniel W. Snyder, circuit assembly Benjamin A. Garcia, and Douglas C. Wallace Pranav Sharma, Pinar Mesci, Cassiano Carromeu, Daniel R. McClatchy, Lucio Schiapparelli, John R. Yates III, Alysson R. See Commentary on page 15763 Muotri, and Hollis T. Cline 16095 Temporal evolution of beta bursts in the parkinsonian MEDICAL SCIENCES cortical and basal ganglia network 16036 Human species-specific loss of CMP-N- Hayriye Cagnan, Nicolas Mallet, Christian K. E. Moll, acetylneuraminic acid hydroxylase enhances Alessandro Gulberti, Abbey B. Holt, Manfred Westphal, atherosclerosis via intrinsic and extrinsic mechanisms Christian Gerloff, Andreas K. Engel, Wolfgang Hamel, Peter J. Kunio Kawanishi, Chirag Dhar, Raymond Do, Nissi Varki, Magill, Peter Brown, and Andrew Sharott Philip L. S. M. Gordts, and Ajit Varki PHYSIOLOGY MICROBIOLOGY 16105 Remote sensing and signaling in kidney proximal 15774 Genome editing using the endogenous type I tubules stimulates gut microbiome-derived CRISPR-Cas system in Lactobacillus crispatus organic anion secretion Claudio Hidalgo-Cantabrana, Yong Jun Goh, Meichen Pan, Jitske Jansen, Katja Jansen, Ellen Neven, Ruben Poesen, Amr Rosemary Sanozky-Dawes, and Rodolphe Barrangou Othman, Alain van Mil, Joost Sluijter, Javier Sastre Torano, See Profile on page 15754 Esther A. Zaal, Celia R. Berkers, Diederik Esser, Harry J. 16046 Epstein–Barr virus reprograms human B lymphocytes Wichers, Karin van Ede, Majorie van Duursen, Ste´phane Burtey, Marianne C. Verhaar, Bjo¨rn Meijers, and Rosalinde Masereeuw immediately in the prelatent phase of infection Paulina Mrozek-Gorska, Alexander Buschle, Dagmar Pich, 16111 BDNF is a mediator of glycolytic fiber-type Thomas Schwarzmayr, Ron Fechtner, Antonio Scialdone, specification in mouse skeletal muscle and Wolfgang Hammerschmidt Julien Delezie, Martin Weihrauch, Geraldine Maier, Rocı´o Tejero, Daniel J. Ham, Jonathan F. Gill, Bettina NEUROSCIENCE Karrer-Cardel, Markus A. Ru¨egg, Lucı´a Tabares, and Christoph Handschin 15855 Developmental topography of cortical thickness during infancy PLANT BIOLOGY Fan Wang, Chunfeng Lian, Zhengwang Wu, Han Zhang, Tengfei Li, Yu Meng, Li Wang, Weili Lin, Dinggang Shen, 16121 The Rho-family GTPase OsRac1 controls rice grain and Gang Li size and yield by regulating cell division 15861 The neural representation of facial-emotion Ying Zhang, Yan Xiong, Renyi Liu, Hong-Wei Xue, and Zhenbiao Yang categories reflects conceptual structure Jeffrey A. Brooks, Junichi Chikazoe, Norihiro Sadato, 16127 The flowering hormone florigen accelerates and Jonathan B. Freeman secondary cell wall biogenesis to harmonize vascular 16056 Prestimulus feedback connectivity biases the content maturation with reproductive development of visual experiences Akiva Shalit-Kaneh, Tamar Eviatar-Ribak, Guy Horev, Naomi Suss, Roni Aloni, Yuval Eshed, and Eliezer Lifschitz Elie Rassi, Andreas Wutz, Nadia Mu¨ller-Voggel, and Nathan Weisz PSYCHOLOGICAL AND COGNITIVE SCIENCES 16062 Methodology and theoretical basis of forward genetic screening for sleep/wakefulness in mice 16137 Gain control of saccadic eye movements Chika Miyoshi, Staci J. Kim, Takahiro Ezaki, Aya Ikkyu, Noriko is probabilistic Hotta-Hirashima, Satomi Kanno, Miyo Kakizaki, Mana Yamada, Matteo Lisi, Joshua A. Solomon, and Michael J. Morgan Shigeharu Wakana, Masashi Yanagisawa, and Hiromasa Funato SYSTEMS BIOLOGY 16068 Transsynaptic Fish-lips signaling prevents misconnections 15830 Membraneless polyester microdroplets as primordial between nonsynaptic partner olfactory neurons compartments at the origins of life Qijing Xie, Bing Wu, Jiefu Li, Chuanyun Xu, Hongjie Li, David J. Tony Z. Jia, Kuhan Chandru, Yayoi Hongo, Rehana Afrin, Luginbuhl, Xin Wang, Alex Ward, and Liqun Luo Tomohiro Usui, Kunihiro Myojo, and H. James Cleaves II 16074 Increased ER–mitochondria tethering promotes 16143 Homotypic cooperativity and collective binding are axon regeneration determinants of bHLH specificity and function Soyeon Lee, Wei Wang, Jinyeon Hwang, Uk Namgung, Christian A. Shively, Jiayue Liu, Xuhua Chen, Kaiser Loell, and Kyung-Tai Min and Robi D. Mitra

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