June 18, 2019 u vol. 116 u no. 25

From the Cover

12353 Regulating biomineralization in echinoderms 12156 Superconducting copper oxide 12244 Adapting to increasing social diversity 12261 Economic impacts of melting Greenland ice sheet 12468 Chlamydia trachomatis and ammonia production

Contents

THIS WEEK IN PNAS Cover image: Pictured is a live sea 12113 In This Issue urchin embryo at the prism stage stained with a membrane tracker (gray) and a calcium-binding dye (false color blue). NEWS FEATURE—An in-depth look at trending science issues Miri Morgulis et al. examined gene 12116 Probing the limits of “evolutionary rescue” regulation and mineral uptake and Amy McDermott deposition as skeletons formed in the embryos. The authors found that vascular endothelial growth factor QNAS (VEGF) signaling activated hundreds 12121 QnAs with Mitchell A. Lazar of genes, including genes for Sandeep Ravindran biomineralization and vascularization. The authors also found similarities See Inaugural Article on page 12147 between VEGF-induced mechanisms 12123 QnAs with Hidde L. Ploegh and those that influence vascularization Prashant Nair in vertebrates. Additional similarities See Inaugural Article on page 7624 in issue 16 of volume 116 suggested that vertebrate vascularization and sea urchin spiculogenesis evolved from an PROFILE ancestral VEGF-driven program adapted 12126 Profile of David D. Ginty for biomineralization in echinoderms. Sandeep Ravindran See the article by Morgulis et al. on See Inaugural Article on page 9168 in issue 19 of volume 116 pages 12353–12362. Image courtesy of Smadar Ben-Tabou de-Leon, Tsvia Gildor, and Miri Morgulis. COMMENTARIES

12129 A different branch of the high Tc family? D. J. Scalapino See companion article on page 12156 12131 Adaptation to diversity: Individual and societal processes Linda R. Tropp See companion article on page 12244 12134 Valuing the Greenland ice sheet and other complex geophysical phenomena William A. Pizer See companion article on page 12261 12136 How Chlamydia trachomatis conquered gut microbiome-derived antimicrobial compounds and found a new home in the eye Arkaprabha Banerjee and David E. Nelson See companion article on page 12468

Free online through the PNAS open access option. PNAS u June 18, 2019 u vol. 116 u no. 25 u iii–vii Downloaded by guest on September 29, 2021 ENGINEERING LETTERS 12183 Intraarticular injection of relaxin-2 alleviates 12139 Misallocation of mycorrhizal traits leads to shoulder arthrofibrosis misleading results William A. Blessing, Stephen M. Okajima, M. Belen Cubria, Leho Tedersoo, Saleh Rahimlou, and Mark Brundrett Juan C. Villa-Camacho, Miguel Perez-Viloria, Patrick M. 12141 Reply to Tedersoo et al.: Plant species within the Williamson, Angie N. Sabogal, Sebastian Suarez, Lay-Hong same family or genus can have different Ang, Suzanne White, Evelyn Flynn, Edward K. Rodriguez, mycorrhizal types? Mark W. Grinstaff, and Ara Nazarian Tao Sun, Hongguang Zhang, and Zhengwen Wang 12193 Hydrodynamics control shear-induced pattern 12143 Populations are not declining and food webs are not formation in attractive suspensions collapsing at the Luquillo Experimental Forest Zsigmond Varga, Vincent Grenard, Stefano Pecorario, Nicolas Taberlet, Vincent Dolique, Se´bastien Manneville, Thibaut M. R. Willig, L. Woolbright, S. J. Presley, T. D. Schowalter, Divoux, Gareth H. McKinley, and James W. Swan R. B. Waide, T. Heartsill Scalley, J. K. Zimmerman, G. Gonza´lez, and A. E. Lugo PHYSICS 12145 Reply to Willig et al.: Long-term population trends in the Luquillo Rainforest 12199 Magnetic field-induced intermediate quantum spin liquid with a spinon Fermi surface Brad Lister and Andres Garcia Niravkumar D. Patel and Nandini Trivedi 12204 Crossover from interaction to driven regimes in INAUGURAL ARTICLE quantum vortex reconnections 12147 SR9009 has REV-ERB–independent effects on cell Luca Galantucci, Andrew W. Baggaley, Nick G. Parker, and Carlo F. Barenghi proliferation and metabolism Pieterjan Dierickx, Matthew J. Emmett, Chunjie Jiang, Kahealani Uehara, Manlu Liu, Marine Adlanmerini, and Mitchell A. Lazar SUSTAINABILITY SCIENCE See QnAs on page 12121 12212 Renewable CO2 recycling and synthetic fuel production in a marine environment Bruce D. Patterson, Frode Mo, Andreas Borgschulte, Magne BRIEF REPORT Hillestad, Fortunat Joos, Trygve Kristiansen, Svein Sunde, and Jeroen A. van Bokhoven 12153 A bacterial isolate from the Black Sea oxidizes sulfide with manganese(IV) oxide Jan V. Henkel, Olaf Dellwig, Falk Pollehne, Daniel P. R. SOCIAL SCIENCES Herlemann, Thomas Leipe, and Heide N. Schulz-Vogt ANTHROPOLOGY 12220 Reconstructing sexual divisions of labor from PHYSICAL SCIENCES fingerprints on Ancestral Puebloan pottery APPLIED PHYSICAL SCIENCES John Kantner, David McKinney, Michele Pierson, and Shaza Wester 12156 Superconductivity in a unique type of copper oxide W. M. Li, J. F. Zhao, L. P. Cao, Z. Hu, Q. Z. Huang, X. C. 12226 Temple occupation and the tempo of collapse at Wang, Y. Liu, G. Q. Zhao, J. Zhang, Q. Q. Liu, R. Z. Yu, Angkor Wat, Cambodia Y. W. Long, H. Wu, H. J. Lin, C. T. Chen, Z. Li, Z. Z. Gong, Alison K. Carter, Miriam T. Stark, Seth Quintus, Yijie Zhuang, Z. Guguchia, J. S. Kim, G. R. Stewart, Y. J. Uemura, S. Uchida, Hong Wang, Piphal Heng, and Rachna Chhay and C. Q. Jin See Commentary on page 12129 ECONOMIC SCIENCES 12232 Mangroves shelter coastal economic activity BIOPHYSICS AND COMPUTATIONAL BIOLOGY from cyclones 12161 The base pair-scale diffusion of nucleosomes Jacob P. Hochard, Stuart Hamilton, and Edward B. Barbier modulates binding of transcription factors ENVIRONMENTAL SCIENCES Sergei Rudnizky, Hadeel Khamis, Omri Malik, Philippa Melamed, and Ariel Kaplan 12238 Evolution of global marine fishing fleets and the response of fished resources Yannick Rousseau, Reg A. Watson, Julia L. Blanchard, CHEMISTRY and Elizabeth A. Fulton 12167 Ratiometric two-photon microscopy reveals attomolar copper buffering in normal and Menkes mutant cells PSYCHOLOGICAL AND COGNITIVE SCIENCES M. Thomas Morgan, Daisy Bourassa, Shefali Harankhedkar, 12566 Elephants have a nose for quantity Adam M. McCallum, Stephanie A. Zlatic, Jenifer S. Calvo, Joshua M. Plotnik, Daniel L. Brubaker, Rachel Dale, Lydia N. Gabriele Meloni, Victor Faundez, and Christoph J. Fahrni Tiller, Hannah S. Mumby, and Nicola S. Clayton

EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES SOCIAL SCIENCES 2 1 12173 H/ H variation in microbial lipids is controlled by 12244 Humans adapt to social diversity over time NADPH metabolism Miguel R. Ramos, Matthew R. Bennett, Douglas S. Massey, Reto S. Wijker, Alex L. Sessions, Tobias Fuhrer, and Michelle Phan and Miles Hewstone 12261 Economics of the disintegration of the Greenland See Commentary on page 12131 ice sheet 12250 Segregation through the multiscalar lens William Nordhaus Madalina Olteanu, Julien Randon-Furling, See Commentary on page 12134 and William A. V. Clark

iv u www.pnas.org Contents Downloaded by guest on September 29, 2021 12255 The promise and peril of sexual harassment programs 12327 Regulation of Caenorhabditis elegans neuronal Frank Dobbin and Alexandra Kalev polarity by heterochronic genes Maria Armakola and Gary Ruvkun SUSTAINABILITY SCIENCE ECOLOGY 12261 Economics of the disintegration of the Greenland – ice sheet 12337 A global model of island species area relationships William Nordhaus Thomas J. Matthews, Franc¸ois Rigal, Kostas A. Triantis, and Robert J. Whittaker See Commentary on page 12134 ENVIRONMENTAL SCIENCES BIOLOGICAL SCIENCES 12173 2H/1H variation in microbial lipids is controlled by NADPH metabolism ANTHROPOLOGY Reto S. Wijker, Alex L. Sessions, Tobias Fuhrer, and Michelle Phan 12220 Reconstructing sexual divisions of labor from fingerprints on Ancestral Puebloan pottery EVOLUTION John Kantner, David McKinney, Michele Pierson, 12343 On the occurrence of cytochrome P450 in viruses and Shaza Wester David C. Lamb, Alec H. Follmer, Jared V. Goldstone, David R. Nelson, Andrew G. Warrilow, Claire L. Price, APPLIED BIOLOGICAL SCIENCES Marie Y. True, Steven L. Kelly, Thomas L. Poulos, 12270 Fast-moving bat ears create informative Doppler shifts and John J. Stegeman Xiaoyan Yin and Rolf Mu¨ller 12353 Possible cooption of a VEGF-driven tubulogenesis program for biomineralization in echinoderms BIOCHEMISTRY Miri Morgulis, Tsvia Gildor, Modi Roopin, Noa Sher, 12161 The base pair-scale diffusion of nucleosomes Assaf Malik, Maya Lalzar, Monica Dines, Shlomo modulates binding of transcription factors Ben-Tabou de-Leon, Lama Khalaily, and Smadar Ben-Tabou de-Leon Sergei Rudnizky, Hadeel Khamis, Omri Malik, Philippa Melamed, and Ariel Kaplan 12363 Ancient Yersinia pestis genomes from across Western Europe reveal early diversification 12167 Ratiometric two-photon microscopy reveals attomolar during the First Pandemic (541–750) copper buffering in normal and Menkes mutant cells Marcel Keller, Maria A. Spyrou, Christiana L. Scheib, Gunnar M. Thomas Morgan, Daisy Bourassa, Shefali Harankhedkar, U. Neumann, Andreas Kro¨pelin, Brigitte Haas-Gebhard, Bernd Adam M. McCallum, Stephanie A. Zlatic, Jenifer S. Calvo, Pa¨ffgen, Jochen Haberstroh, Albert Ribera i Lacomba, Claude Gabriele Meloni, Victor Faundez, and Christoph J. Fahrni Raynaud, Craig Cessford, Raphae¨l Durand, Peter Stadler, 12275 Inward-facing conformation of a multidrug resistance Kathrin Na¨gele, Jessica S. Bates, Bernd Trautmann, Sarah A. MATE family transporter Inskip, Joris Peters, John E. Robb, Toomas Kivisild, Dominique Sandra Zakrzewska, Ahmad Reza Mehdipour, Viveka Castex, Michael McCormick, Kirsten I. Bos, Michaela Harbeck, Nand Malviya, Tsuyoshi Nonaka, Juergen Koepke, Cornelia Alexander Herbig, and Johannes Krause Muenke, Winfried Hausner, Gerhard Hummer, Schara Safarian, 12373 Adult sex ratio influences mate choice in and Hartmut Michel Darwin’s finches 12285 Hsp90 of E. coli modulates assembly of FtsZ, the Peter R. Grant and B. Rosemary Grant bacterial tubulin homolog 12383 A major role for noncoding regulatory mutations in Anuradha Balasubramanian, Monica Markovski, Joel R. the evolution of enzyme activity Hoskins, Shannon M. Doyle, and Sue Wickner David W. Loehlin, Jesse R. Ames, Kathy Vaccaro, and Sean B. Carroll BIOPHYSICS AND COMPUTATIONAL BIOLOGY 12295 Unique transmembrane domain interactions GENETICS differentially modulate integrin αvβ3 and 12390 Preformed chromatin topology assists transcriptional αIIbβ3 function robustness of Shh during limb development Rustem I. Litvinov, Marco Mravic, Hua Zhu, John W. Weisel, Christina Paliou, Philine Guckelberger, Robert Scho¨pflin, William F. DeGrado, and Joel S. Bennett Verena Heinrich, Andrea Esposito, Andrea M. Chiariello, 12301 Unfolded states under folding conditions Simona Bianco, Carlo Annunziatella, Johannes Helmuth,  accommodate sequence-specific conformational Stefan Haas, Ivana Jerkovic, Norbert Brieske, Lars Wittler, preferences with random coil-like dimensions Bernd Timmermann, Mario Nicodemi, Martin Vingron, Stefan Mundlos, and Guillaume Andrey Ivan Peran, Alex S. Holehouse, Isaac S. Carrico, Rohit V. Pappu, Osman Bilsel, and Daniel P. Raleigh 12400 Building bridges to move recombination complexes Emeline Dubois, Arnaud De Muyt, Jessica L. Soyer, Karine CELL BIOLOGY Budin, Mathieu Legras, Tristan Piolot, Robert Debuchy, Nancy Kleckner, Denise Zickler, and Eric Espagne 12311 LSD1 destabilizes FBXW7 and abrogates FBXW7 functions independent of its demethylase activity IMMUNOLOGY AND INFLAMMATION Huiyin Lan, Mingjia Tan, Qiang Zhang, Fei Yang, Siyuan Wang, 12410 TOX and TOX2 transcription factors cooperate Hua Li, Xiufang Xiong, and Yi Sun with NR4A transcription factors to impose + CD8 T cell exhaustion DEVELOPMENTAL BIOLOGY Hyungseok Seo, Joyce Chen, Edahı´ Gonza´lez-Avalos, 12321 Hypoxia induces the dormant state in oocytes Daniela Samaniego-Castruita, Arundhoti Das, through expression of Foxo3 Yueqiang H. Wang, Isaac F. Lo´pez-Moyado, So Shimamoto, Yohei Nishimura, Go Nagamatsu, Norio Romain O. Georges, Wade Zhang, Atsushi Onodera, Hamada, Haruka Kita, Orie Hikabe, Nobuhiko Hamazaki, Cheng-Jang Wu, Li-Fan Lu, Patrick G. Hogan, Avinash and Katsuhiko Hayashi Bhandoola, and Anjana Rao

Contents PNAS u June 18, 2019 u vol. 116 u no. 25 u v Downloaded by guest on September 29, 2021 12416 Dual mechanisms of posttranscriptional regulation of 12494 ANO1/TMEM16A regulates process maturation in Tet2 by Let-7 microRNA in macrophages radial glial cells in the developing brain Shuai Jiang, Wei Yan, Shizhen Emily Wang, Gyu-Sang Hong, Sung Hoon Lee, Byeongjun Lee, Jae Hyouk and David Baltimore Choi, Soo-Jin Oh, Yongwoo Jang, Eun Mi Hwang, Hyungsup 12422 Protein phosphatase 2A has an essential role in Kim, Jooyoung Jung, In-Beom Kim, and Uhtaek Oh promoting thymocyte survival during selection 12500 UBE3A-mediated PTPA ubiquitination and degradation Mingzhu Zheng, Dan Li, Zhishan Zhao, Dmytro Shytikov, regulate PP2A activity and dendritic spine morphology Qin Xu, Xuexiao Jin, Jingjing Liang, Jun Lou, Songquan Jie Wang, Sen-Sen Lou, Tingting Wang, Rong-Jie Wu, Guangying Wu, Lie Wang, Hu Hu, Yiting Zhou, Xiang Gao, and Linrong Lu Li, Miao Zhao, Bin Lu, Yi-Yan Li, Jing Zhang, Xuewen Cheng, 12428 Olfactory sensory neurons mediate ultrarapid Ya Shen, Xing Wang, Zhi-Chuan Zhu, Ming-Jie Li, Toru Takumi, Hui Yang, Xiang Yu, Lujian Liao, and Zhi-Qi Xiong antiviral immune responses in a TrkA-dependent manner 12506 Routing information flow by separate neural “ Ali Sepahi, Aurora Kraus, Elisa Casadei, Christopher A. synchrony frequencies allows for functionally Johnston, Jorge Galindo-Villegas, Cecelia Kelly, Diana labeled lines” in higher primate cortex Garcı´a-Moreno, Pilar Mun˜oz, Victoriano Mulero, Mohammad Bagher Khamechian, Vladislav Kozyrev, Stefan Mar Huertas, and Irene Salinas Treue, Moein Esghaei, and Mohammad Reza Daliri 12516 NRF2/ARE pathway negatively regulates BACE1 MEDICAL SCIENCES expression and ameliorates cognitive deficits 12183 Intraarticular injection of relaxin-2 alleviates in mouse Alzheimer’s models shoulder arthrofibrosis Gahee Bahn, Jong-Sung Park, Ui Jeong Yun, Yoon Jee Lee, Yuri William A. Blessing, Stephen M. Okajima, M. Belen Cubria, Choi, Jin Su Park, Seung Hyun Baek, Bo Youn Choi, Yoon Suk Cho, Juan C. Villa-Camacho, Miguel Perez-Viloria, Patrick M. Hark Kyun Kim, Jihoon Han, Jae Hoon Sul, Sang-Ha Baik, Jinhwan Williamson, Angie N. Sabogal, Sebastian Suarez, Lay-Hong Lim, Nobunao Wakabayashi, Soo Han Bae, Jeung-Whan Han, Ang, Suzanne White, Evelyn Flynn, Edward K. Rodriguez, Thiruma V. Arumugam, Mark P. Mattson, and Dong-Gyu Jo Mark W. Grinstaff, and Ara Nazarian 12524 Specific factors in blood from young but not old mice 12437 Boundary mode lubrication of articular cartilage with directly promote synapse formation and a biomimetic diblock copolymer NMDA-receptor recruitment Zhexun Sun, Elizabeth Feeney, Ya Guan, Sierra G. Cook, Kathlyn J. Gan and Thomas C. Su¨dhof Delphine Gourdon, Lawrence J. Bonassar, and David Putnam 12442 JAK/STAT inhibition in macrophages promotes PHARMACOLOGY therapeutic resistance by inducing expression 12147 SR9009 has REV-ERB–independent effects on cell of protumorigenic factors proliferation and metabolism Emily A. Irey, Chelsea M. Lassiter, Nicholas J. Brady, Pavlina Pieterjan Dierickx, Matthew J. Emmett, Chunjie Jiang, Kahealani Chuntova, Ying Wang, Todd P. Knutson, Christine Henzler, Uehara, Manlu Liu, Marine Adlanmerini, and Mitchell A. Lazar Thomas S. Chaffee, Rachel I. Vogel, Andrew C. Nelson, See QnAs on page 12121 Michael A. Farrar, and Kathryn L. Schwertfeger 12452 Hypoxia-induced switch in SNAT2/SLC38A2 PLANT BIOLOGY regulation generates endocrine resistance in 12534 The Cdk1/Cdk2 homolog CDKA;1 controls the breast cancer recombination landscape in Arabidopsis Matteo Morotti, Esther Bridges, Alessandro Valli, Hani Erik Wijnker, Hirofumi Harashima, Katja Mu¨ller, Pablo Choudhry, Helen Sheldon, Simon Wigfield, Nicki Gray, Parra-Nun˜ez, C. Bastiaan de Snoo, Jose van de Belt, Nico Christos E. Zois, Fiona Grimm, Dylan Jones, Eugene J. Teoh, Dissmeyer, Martin Bayer, Monica Pradillo, and Arp Schnittger Wei-Chen Cheng, Simon Lord, Dimitrios Anastasiou, Syed 12540 Arabidopsis ABCG28 is required for the apical Haider, Alan McIntyre, Deborah C. I. Goberdhan, Francesca accumulation of reactive oxygen species in Buffa, and Adrian L. Harris growing pollen tubes MICROBIOLOGY Thanh Ha Thi Do, Hyunju Choi, Michael Palmgren, Enrico Martinoia, Jae-Ung Hwang, and Youngsook Lee 12462 Salmonella biofilms program innate immunity for persistence in Caenorhabditis elegans 12550 Engineering the phototropin photocycle improves Stuti K. Desai, Anup Padmanabhan, Sharvari Harshe, Ronen photoreceptor performance and plant Zaidel-Bar, and Linda J. Kenney biomass production Jaynee E. Hart, Stuart Sullivan, Paweł Hermanowicz, Jan 12468 Ammonia generation by tryptophan synthase Petersen, L. Aranzazu´ Diaz-Ramos, David J. Hoey, Justyna drives a key genetic difference between genital Łabuz, and John M. Christie and ocular Chlamydia trachomatis isolates 12558 Plant-derived coumarins shape the composition of an Shardulendra P. Sherchand and Ashok Aiyar Arabidopsis synthetic root microbiome See Commentary on page 12136 Mathias J. E. E. E. Voges, Yang Bai, Paul Schulze-Lefert, 12478 Primary structural differences at residue 226 of deer and Elizabeth S. Sattely and elk PrP dictate selection of distinct CWD prion strains in gene-targeted mice PSYCHOLOGICAL AND COGNITIVE SCIENCES Jifeng Bian, Jeffrey R. Christiansen, Julie A. Moreno, Sarah J. 12566 Elephants have a nose for quantity Kane, Vadim Khaychuk, Joseph Gallegos, Sehun Kim, Joshua M. Plotnik, Daniel L. Brubaker, Rachel Dale, Lydia N. and Glenn C. Telling Tiller, Hannah S. Mumby, and Nicola S. Clayton

NEUROSCIENCE SUSTAINABILITY SCIENCE 12488 Stress transforms lateral habenula reward responses 12238 Evolution of global marine fishing fleets and the into punishment signals response of fished resources Steven J. Shabel, Chenyu Wang, Bradley Monk, Sage Aronson, Yannick Rousseau, Reg A. Watson, Julia L. Blanchard, and Roberto Malinow and Elizabeth A. Fulton

vi u www.pnas.org Contents Downloaded by guest on September 29, 2021 NEUROSCIENCE CORRECTIONS 12574 Regulation of myelin structure and conduction ENGINEERING velocity by perinodal astrocytes 12572 Computer simulations suggest that prostate Dipankar J. Dutta, Dong Ho Woo, Philip R. Lee, enlargement due to benign prostatic hyperplasia Sinisa Pajevic, Olena Bukalo, William C. Huffman, mechanically impedes prostate cancer growth Hiroaki Wake, Peter J. Basser, Shahriar SheikhBahaei, Vanja Lazarevic, Jeffrey C. Smith, Guillermo Lorenzo, Thomas J. R. Hughes, Pablo and R. Douglas Fields Dominguez-Frojan, Alessandro Reali, and Hector Gomez

MICROBIOLOGY PLANT BIOLOGY 12573 Activation of RNase L is dependent on OAS3 expression 12575 Processing bodies control the selective translation during infection with diverse human viruses for optimal development of Arabidopsis Yize Li, Shuvojit Banerjee, Yuyan Wang, Stephen A. Goldstein, young seedlings Beihua Dong, Christina Gaughan, Robert H. Silverman, Geng-Jen Jang, Jun-Yi Yang, Hsu-Liang Hsieh, and Susan R. Weiss and Shu-Hsing Wu

Contents PNAS u June 18, 2019 u vol. 116 u no. 25 u vii Downloaded by guest on September 29, 2021