Fine Read­ing: A Col­lec­tion of No­table Pub­li­ca­tions from 2017

by Roberto and Elio

Source

As this past year came to a close we wanted to get a col­lection of salient pub­li­ca­tions to share with our STC au­di­ence. To as­sem­ble this col­lec­tion, we asked a num­ber of our friends and col­leagues from many lo­ca­tions across the globe to se­lect a pub­li­ca­tion from 2017 that they found par­tic­u­larly fas­ci­nat­ing. Along with pro­vid­ing the ci­ta­tion, we asked them very briefly de­scribe what was it about that pub­li­ca­tion that ex­cited them. The eclec­tic na­ture of the col­lec­tion that we share be­low is tes­ta­ment to the re­markable di­ver­sity of ex­tremely ex­cit­ing re­search that is cur­rently be­ing done in the mi­cro­bial sci­ences. Our sense is that this list very much sup­ports our view that there was never a bet­ter time to con­sider those mar­velous "small things" than the pre­sent. Af­ter con­sid­er­ing this list, we in­vite each and every one of our read­ers to con­tribute (through our com­ment sec­tion) their own se­lec­tion of a fas­ci­nat­ing pa­per of 2017.

An­cient bac­te­ria of the Ötzi's mi­cro­biome: a ge­nomic tale from the Cop­per Age

Lugli GA, Mi­lani C, Man­ca­belli L, Tur­roni F, Fer­rario C, Du­ranti S, van Sin­deren D, Ven­tura M. Micro­biome. 2017. 5 (1), 5

These in­ves­ti­ga­tors looked in the gut mi­cro­biota of a "frozen mum­mi­fied hu­man" called the Tyro­le­an Ice­man and found a com­mu­nity pre­dom­i­nated by Clostrid­ium and Pseudomonas species. Pseudomonas spp., in­clud­ing P. veroni  and P. flu­o­rescens, are not typ­i­cally thought of as com­mon gut mi­cro­biota, in­di­cat­ing some po­ten­tial shift in the gut com­mu­ni­ties from this an­ces­tor from ~5000 years ago. Or per­haps this find­ing in­di­cates that the DNA of Clostrid­ium and Pseudomonas species is par­tic­u­larly sta­ble in these con­di­tions. Ei­ther way, it was an in­trigu­ing find­ing.

George O'Toole   De­part­ment of Mi­cro­bi­ol­ogy and Im­munol­ogy, Geisel School of Med­i­cine at Dart­mouth, Hanover, NH, United States.

 

Long-Chain Alkyl Cyanides: Un­prece­dented Volatile Com­pounds Re­leased by Pseudomonas and Mi­cromono­spora Bac­te­ria

Montes Vi­dal D, von Ry­mon-Lip­in­ski AL, Ravella S, Groen­hagen U, Her­rmann J, Zabu­ran­nyi N, Zarbin PH, Varadara­jan AR, Ahrens CH, Weis­skopf L, Müller R, Schulz S. Angew Chem Int Ed Engl. 2017. 56 (15), 4342 − 4346

The biosyn­thetic ar­se­nal en­coded by mi­croor­gan­isms still con­tin­ues to sur­prise us even in bac­te­ria from com­mer­cial col­lec­tions. The char­ac­ter­i­za­tion and biosyn­the­sis of new volatile alkyl cyanides was de­ter­mined in a se­ries of el­e­gant ex­per­i­ments, and their an­timi­cro­bial ac­tiv­ity sug­gests a role in in­ter­species com­mu­ni­ca­tion. What also called my at­ten­tion: the pa­per in­volves the collabora­tion be­tween Ger­man and Brazil­ian sci­en­tists, a won­der­ful ex­am­ple of in­ter­na­tional re­search.

Mônica T. Pupo   De­part­ment of Phar­ma­ceu­ti­cal Sci­ences, School of Phar­ma­ceu­ti­cal Sci­ences of Ribeirão Preto, Ribeirão Preto, SP, Brasil.

 

Sec­ond mes­sen­ger-me­di­ated tac­tile re­sponse by a bac­te­r­ial ro­tary mo­tor

Hug I, Desh­pande S, Sprecher KS, Pfohl T, Je­nal U. Sci­ence. 2017. 358 (6362), 531 − 534

The rea­son I find this pa­per fas­ci­nat­ing is that in my view it pro­vides the first di­rect ev­i­dence for con­tact sur­face sens­ing al­though many other pub­li­ca­tions have toyed with this con­cept. How­ever, all pre­vi­ous stud­ies were us­ing in­di­rect re­porter as­says, i.e. gene tran­scrip­tion and un­con­trolled sur­faces (i.e. agar of dif­fer­ent con­cen­tra­tions). So, al­though the idea of con­tact sens­ing was appea­ling, it was not re­ally demon­strated. Here, us­ing a new mi­croflu­idic as­say, the au­thors show that sur­face-in­duced in­ter­fer­ences of the fla­gella mo­tor gen­er­ate the rapid pro­duc­tion of c‑di-GMP by a mo­tor-as­so­ci­ated cy­clase, which in turns rapidly in­duces ac­ti­va­tion of a poly­sac­cha­ride ad­hesin by al­losteric con­trol. The en­tire cas­cade is char­ac­ter­ized in this very el­e­gant piece of work.

Tâm Mignot   Lab­o­ra­toire de Chimie Bac­téri­enne, CNRS-Aix Mar­seille Uni­ver­sity UMR7283, In­sti­tut de Mi­cro­bi­olo­gie de la Méditer­ranée, Mar­seille, France.

 

Mi­cro­bial mass move­ments

Zhu YG, Gillings M, Si­monet P, Stekel D, Ban­wart S, Penue­las J. Sci­ence. 2017. 357 (6356), 1099 − 1100

De­spite our grow­ing aware­ness of the ef­fects that hu­mans have on our planet and the environ­ment, we have yet to as­sess how our ac­tiv­i­ties af­fect mi­cro­bial com­mu­ni­ties on a global scale and what these changes can mean in terms of ecosys­tem health and main­te­nance. In this per­spec­tive, the au­thors il­lus­trate how hu­man ac­tiv­i­ties have al­tered the dy­nam­ics of mi­cro­bial move­ment on a mas­sive scale. Such ac­tiv­i­ties can change mi­cro­bial abun­dances and dis­tri­b­u­tion and have a sig­nificant im­pact on global health and sus­tain­abil­ity.

María Mer­cedes Zam­brano   Cen­ter for Ge­nomics and Bioin­for­mat­ics of Ex­treme En­vi­ron­ments (Gebix), Cor­po­ración Cor­pogen Re­search Cen­ter, Bo­gotá, Colom­bia.

 

Prophages and Growth Dy­nam­ics Con­found Ex­per­i­men­tal Re­sults with An­tibi­otic-Tol­er­ant Per­sis­ter Cells

Harms A, Fino C, Sørensen MA, Sem­sey S, Gerdes K. Mbio. 2017. 8 (6), pii: e01964-17

This is my fa­vorite pa­per of 2017 for its high qual­ity, forth­right­ness, and con­tri­tion. Orig­i­nally pub­lished on bioRxiv un­der a more evoca­tive ti­tle "Nasty Prophages and the Dy­nam­ics of An­tibi­otic-Tol­er­ant Per­sis­ter Cells," this pa­per largely negates the au­thors' pre­vi­ous con­clu­sion that toxin-an­ti­toxin sys­tems play a key role in the de­vel­op­ment per­sis­ter cells able to tol­er­ate high concentra­tions of bac­te­ri­o­ci­dal com­pounds. High­light­ing the it­er­a­tive na­ture of sci­ence and the value of skep­ti­cism, even in re­gard to your own work, the au­thors demon­strate that in­fec­tion of mu­tant strains with bac­te­rio­phage φ80 – rather than loss of TA toxin sys­tems – was the un­der­ly­ing cause of an­tibi­otic sen­si­tiv­ity in their pre­vi­ous high pro­file study.

Pe­tra Levin   De­part­ment of Bi­ol­ogy, Wash­ing­ton Uni­ver­sity in St. Louis, St. Louis, MO, United States.

 

De­struc­tion and ref­or­ma­tion of an iron-sul­fur clus­ter dur­ing catal­y­sis by lipoyl syn­thase

Mc­Carthy EL, Booker SJ. Sci­ence. 2017. 358 (6361), 373 − 377

Lipoic acid is an eight-car­bon fatty acid con­tain­ing sulfhydryl groups at C6 and C8 that plays an es­sential role in cen­tral me­tab­o­lism in or­gan­isms rang­ing from bac­te­ria to hu­mans. The en­zyme li­po­yl syn­thetase (LipA) pro­vides both sul­fur atoms from an aux­il­iary [4Fe-4S] clus­ter on the pro­tein that is de­graded dur­ing one turnover in vitro. Mc­Carthy and Booker re­cently found that the Esche­ri­chia coli  iron sul­fur clus­ter car­rier pro­tein NfuA ef­fi­ciently re­con­sti­tutes the aux­il­iary clus­ter du­ring LipA catal­y­sis. These re­sults ex­plain why pa­tients with de­fects in NFU1, the mam­malian ortho­log of NfuA, dis­plays phe­no­types that are con­sis­tent with lipoic acid de­fi­ciency.

Diego de Men­doza   Lab­o­ra­to­rio de Fi­si­ología Mi­cro­biana, Fac­ul­tad de Cien­cias Bio­quími­cas y Far­ma­céu­ti­cas, Uni­ver­si­dad Na­cional de Rosario , Rosario, Ar­gentina.

 

Dy­namic biofilm ar­chi­tec­ture con­fers in­di­vid­ual and col­lec­tive mech­a­nisms of vi­ral protec­tion

Vi­dakovic L, Singh PK, Hart­mann R, Nadell CD, Drescher K. Nat Mi­cro­biol. 2018. 3 (1), 26 − 31

This study re­sults from the pro­duc­tive col­lab­o­ra­tion be­tween Carey Nadell (Dart­mouth) and Knut Drescher (Max Planck In­sti­tute for Ter­res­trial Mi­cro­bi­ol­ogy, Mar­burg). The au­thors show that the ten­dency of bac­te­ria to form biofilms – dense sur­face as­so­ci­ated com­mu­ni­ties – phys­i­cally pro­tects them from phage; specif­i­cally via an amy­loid fi­bre net­work made out­side the cells. This net­work both phys­i­cally blocks phage from en­ter­ing the biofilms – a col­lec­tive mech­a­nism – and binds phage par­ti­cles, pro­tect­ing in­di­vid­ual cells. The com­bi­na­tion of fun­da­men­tal in­sights, de­tailed ex­per­i­ments and beau­ti­ful imag­ing is char­ac­ter­is­tic of these re­searchers and makes the pa­per a plea­sure to read.

Kevin Fos­ter   De­part­ment of Zo­ol­ogy, Uni­ver­sity of Ox­ford, Ox­ford, United King­dom.

 

As­sem­bly of a nu­cleus-like struc­ture dur­ing vi­ral repli­ca­tion in bac­te­ria

Chaikeer­ati­sak V, Nguyen K, Khanna K, Brilot AF, Erb ML, Coker JK, Vav­ilina A, New­ton GL, Buschauer R, Pogliano K, Villa E, Agard DA, Pogliano J. Sci­ence. 2017. 355 (6321), 194 − 197

The au­thors of this ar­ti­cle dis­cov­ered a nu­cleus-like struc­ture formed in Pseudomonas upon its phage in­fec­tion. The sur­pris­ing ob­ser­va­tion with re­gard to the com­part­ment sep­a­rat­ing phage DNA from the cy­to­plasm not only adds so­phis­ti­cated knowl­edge to the de­vel­op­men­tal bi­ol­ogy of phage pro­lif­er­a­tion but makes a stir in the his­tory of eu­kary­otic cells. Could this be the orig­i­nal event lead­ing to the cre­ation of a nu­cleus? The find­ing will stim­u­late the ar­gu­ment whether the en­dosym­bi­otic the­ory is also ap­plic­a­ble to the de­vel­op­ment of the genome-con­tain­ing or­ganelle. Such au­tonomous be­hav­ior of a set of ge­nomic DNA may be the true na­ture dom­i­nat­ing over the con­sti­tu­tion of life­forms.

Kenji Ueda   Life Sci­ence Re­search Cen­ter, Col­lege of Biore­source Sci­ences, Ni­hon Uni­ver­sity, Fu­ji­sawa, Japan.

 

As­sem­bly of a nu­cleus-like struc­ture dur­ing vi­ral repli­ca­tion in bac­te­ria

Chaikeer­ati­sak V, Nguyen K, Khanna K, Brilot AF, Erb ML, Coker JK, Vav­ilina A, New­ton GL, Buschauer R, Pogliano K, Villa E, Agard DA, Pogliano J. As­sem­bly of a nu­cleus-like struc­ture dur­ing vi­ral repli­ca­tion in bac­te­ria. Sci­ence. 2017 Jan 13;355(6321):194–197. doi: 10.1126/science.aal2130. PMID: 28082593; PMCID: PMC6028185.

An ex­cit­ing 2017 pa­per ? I'd choose this pa­per from the Pogliano lab. Here these re­searchers de­scribed the so­phis­ti­cated struc­tural or­ga­ni­za­tion of host cells by a large Pseudomonas phage. Dur­ing lytic repli­ca­tion, this phage cre­ated a pro­tein-bounded com­part­ment – the site of rep­li­ca­tion and tran­scrip­tion of its DNA. Empty cap­sids that as­sem­bled near the cell mem­brane mi­grated to the com­part­ment bor­der and docked there long enough to each be filled with a phage chro­mo­so­me. This en­tire "phage fac­tory" was po­si­tioned mid­cell by dy­namic "spin­dle" fil­a­ments assemb­led from the phage's tubu­lin ho­molog, PhuZ. The cre­ation of such so­phis­ti­cated "vi­ral fac­to­ries" had pre­vi­ously been ob­served only in com­part­men­tal­ized eu­kary­otic cells. In sum, this pa­per re­minds us that phages are so­phis­ti­cated life forms, their ex­clu­sion from the "uni­ver­sal" tree of life notwith­stand­ing.

Merry Youle   Rain­bow Rock, Ocean View, HI, United States.

 

As­gard ar­chaea il­lu­mi­nate the ori­gin of eu­kary­otic cel­lu­lar com­plex­ity

Zaremba-Niedzwiedzka K, Cac­eres EF, Saw JH, Bäck­ström D, Ju­zokaite L, Van­caester E, Seitz KW, Anan­thara­man K, Star­nawski P, Kjeld­sen KU, Stott MB, Nunoura T, Ban­field JF, Schramm A, Baker BJ, Spang A, Et­tema TJ. Na­ture. 2017. 541 (7637), 353 − 358

This con­tri­bu­tion de­scribes pro­teins of eu­kary­otes as be­ing found in groups deeply em­bed­ded in the Ar­chaea. This ar­ti­cle and some other sim­i­lar ar­ti­cles this year have cre­ated a firestorm of a de­bate about whether there are two do­mains — Ar­chaea and Bac­te­ria or three, Ar­chaea, Bac­te­ria and Eu­karya. The data are pretty con­vinc­ing for two do­mains.

Mar­garet Mc­Fall-Ngai   Pa­cific Bio­sciences Re­search Cen­ter, Uni­ver­sity of Hawaii at Manoa, Hon­olulu, HI, United States.

 

Cou­pling be­tween dis­tant biofilms and emer­gence of nu­tri­ent time-shar­ing

Liu J, Mar­tinez-Cor­ral R, Prindle A, Lee DD, Larkin J, Ga­balda-Sagarra M, Gar­cia-Ojalvo J, Süel GM. Sci­ence. 2017. 356 (6338), 638 − 642

This pa­per gets my vote for pa­per of the year. The au­thors found that phase shift­ing of neu­ron-like os­cil­la­tions fa­cil­i­tates co­op­er­a­tion be­tween two bac­te­r­ial pop­u­la­tions. This study is won­der­ful for at least two rea­sons. First, it is a bril­liant ex­am­ple of how bac­te­ria are ca­pa­ble of sur­pris­ingly com­plex com­mu­ni­ca­tion and be­hav­ior. Sec­ond, this study sup­ports my sus­pi­cion that there is a global ca­bal of mi­crobes form­ing a vast neural net­work in soils and ma­rine sed­i­ments that dwarfs our puny hu­man brains.

David Lip­son   De­part­ment of Bi­ol­ogy, San Diego State Uni­ver­sity, San Diego, CA, United States.

 

Host-se­lected mu­ta­tions con­verg­ing on a global reg­u­la­tor drive an adap­tive leap to­wards sym­bio­sis in bac­te­ria

Pankey SM, Fox­all RL, Ster IM, Perry LA, Schus­ter BM, Don­ner RA, Coyle M, Cooper VS, Whistler CA. Elife. 2017. 6, pii: e24414

The sym­bio­sis be­tween bi­o­lu­mi­nes­cent Vib­rio fis­cheri and squid con­tin­ues to re­veal in­trigu­ing in­sights into the in­tri­cate dance be­tween sym­bi­otic bac­te­ria and their an­i­mal hosts. Mu­ta­tions in a sin­gle gene used for sig­nal­ing (binK) were suf­fi­cient to trans­form V. fis­cheri that were poor at co­loni­zing squid into su­per sym­bionts. How fas­ci­nat­ing that it takes so lit­tle to be­come BFF (best friends for­ever).......

Nicole Du­bilier   Sym­bio­sis De­part­ment, Max Planck In­sti­tute for Ma­rine Mi­cro­bi­ol­ogy, Bre­men, Ger­many.

 

Acoustic re­porter genes for non­in­va­sive imag­ing of mi­croor­gan­isms in mam­malian hosts

Bour­deau RW, Lee-Gos­selin A, Lak­sh­manan A, Farhadi A, Ku­mar SR, Nety SP, Shapiro MG. Na­ture. 2018. 553 (7686), 86 − 90

In this man­u­script, Shapiro and col­leagues en­gi­neer E. coli and Sal­mo­nella to ex­press genes en­coding the as­sem­bly of gas vesi­cles, and show that the gas-vesi­cle-har­bor­ing cells can be im­aged non-in­va­sively us­ing ul­tra­sound. This man­u­script makes a star­tling and cre­ative leap from gas vesi­cles, es­o­teric struc­tures used to con­trol bac­te­r­ial buoy­ancy, to a new imag­ing modal­ity that has high spa­tial res­o­lu­tion and can pen­e­trate tis­sue. 

Michael Fis­chbach   De­part­ment of Bio­engi­neer­ing, Stan­ford Uni­ver­sity, Stan­ford, CA, United States.

 

Struc­ture of phy­co­bil­i­some from the red alga Grif­fith­sia paci­fica

Zhang J, Ma J, Liu D, Qin S, Sun S, Zhao J, Sui SF Na­ture. 2017. 551 (7678), 57 − 63

The au­thors re­port the struc­ture of the main light-har­vest­ing com­plex in cyanobac­te­ria and red al­gae, the phy­co­bil­i­some, at 3.5 Å res­o­lu­tion us­ing cryo-elec­tron mi­croscopy. This tech­nolog al­lows the study of pro­tein struc­ture at near-atomic res­o­lu­tion and de­ter­mine pro­tein do­main organi­za­tion and amino acid in­ter­ac­tions "just by look­ing at the mi­cro­scope." The dom­i­nat­ing role that X‑ray crys­tal­log­ra­phy has played in struc­tural bi­ol­ogy is now chal­lenged by cryo-elec­tron mi­cro­sco­py, as it does not re­quire mak­ing pro­tein crys­tals, it al­lows the study of pro­tein struc­tures in their na­tive en­vi­ron­ments, in whole cells.

Daniel López   Na­tional Cen­ter for Biotech­nol­ogy, Con­sejo Su­pe­rior de In­ves­ti­ga­ciones Cien­tí­fi­cas, Madrid, Spain.

 

Mat­u­ra­tion of the in­fant res­pi­ra­tory mi­cro­biota, en­vi­ron­men­tal dri­vers and health con­se­quences: a prospec­tive co­hort study.

Bosch AA, de Steen­hui­jsen Piters WA, van Houten MA, Chu M, Bies­broek G, Kool J, Per­net P, de Groot PCM, Eijke­mans MJC, Kei­jser BJF, Sanders EAM, Bo­gaert D. Am J Respir Crit Care Med. 2017. 196 (12), 1582 − 1590

Bosch and col­leagues per­formed a prospec­tive lon­gi­tu­di­nal study of the na­sopha­ryn­geal micro­biota of 112 in­fants dur­ing health and res­pi­ra­tory tract in­fec­tion. Their find­ings point to a com­plex re­la­tion­ship be­tween bac­te­r­ial mi­cro­biota com­po­si­tion, en­vi­ron­men­tal dri­vers and sus­cep­ti­bil­ity to res­pi­ra­tory tract in­fec­tions. They found that route of de­liv­ery, feed­ing route, crowd­ing and an­tibiotic use in­flu­ence com­mu­nity com­po­si­tion. In ad­di­tion, there was an as­so­ci­a­tion be­tween mi­crobiota com­po­si­tion and the num­ber of res­pi­ra­tory tract in­fec­tions in the first year of life.

Kather­ine Lemon   Mi­cro­bi­ol­ogy, The Forsyth In­sti­tute, Cam­bridge, MA, United States.

 

Pollen has a mi­cro­biome: im­pli­ca­tions for plant re­pro­duc­tion, in­sect pol­li­na­tion and hu­man al­ler­gies.

Za­sloff M. En­v­i­ron Mi­cro­biol. 2017. 19 (1), 1 − 2

I agree with the au­thor that it is 'ob­vi­ous' that pollen has its own mi­cro­biome. What ex­cited me about this think piece are the re­search ques­tions posed through­out, and their rel­e­vance to mi­cro­biome in­no­va­tion. The ar­ti­cle also re­minded me, from an aerosol sci­ence and air qual­ity per­spec­tive, of the value of de­vel­op­ing cost-ef­fec­tive tech­nolo­gies to char­ac­ter­ize pollen ecosys­tems. 

Jes­sica Green   In­sti­tute of Ecol­ogy and Evo­lu­tion, Uni­ver­sity of Ore­gon, Eu­gene, OR, United States.

 

A path­way for bi­o­log­i­cal methane pro­duc­tion us­ing bac­te­r­ial iron-only ni­tro­ge­nase.

Zheng Y, Har­ris DF, Yu Z, Fu Y, Poudel S, Led­bet­ter RN, Fixen KR, Yang ZY, Boyd ES, Lid­strom ME, Seefeldt LC, Har­wood CS. Nat Mi­cro­biol. 2018. (pub­lished on­line: Jan 15)

The list of re­mark­able ex­am­ples of non-con­ven­tional sub­strate use by mi­cro­bial met­al­loen­zymes is grow­ing and chang­ing our per­cep­tions of their func­tional po­ten­tial in the en­vi­ron­ment. In an el­e­gant col­lab­o­ra­tion be­tween bac­te­r­ial ge­neti­cists, bio­chemists, and mi­cro­bi­ol­o­gists, Zheng and col­leagues demon­strate ex­panded func­tion­al­ity for the iron-only form of ni­tro­ge­nase, re­veal­ing that this en­zyme not only cat­alyzes ni­tro­gen fix­a­tion, but is also ca­pa­ble of di­rect re­duc­tion of car­bon diox­ide to methane. Re­mark­ably, and of sig­nif­i­cance to mi­cro­bial ecol­o­gists, methane was pro­duced in suf­fi­cient quan­ti­ties to sup­port the growth of a methan­otrophic bac­terium in co-cul­­ture. This de­fies con­ven­tional wis­dom, but as we are learn­ing, mi­cro­bial ecol­ogy has just be­gun to un­veil the di­ver­sity of meta­bolic and col­lab­o­ra­tive pos­si­bil­i­ties on Earth.

Vic­to­ria Or­phan   Di­vi­sion of Ge­o­log­i­cal and Plan­e­tary Sci­ences, Cal­i­for­nia In­sti­tute of Tech­nol­ogy, Pasadena, CA, United States.