skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Sulfate-Reducing Bacteria That Produce Exopolymers Thrive in the Calcifying Zone of a Hypersaline Cyanobacterial Mat

Abstract

Calcifying microbial mats in hypersaline environments are important model systems for the study of the earliest ecosystems on Earth that started to appear more than three billion years ago and have been preserved in the fossil record as laminated lithified structures known as stromatolites. It is believed that sulfate-reducing bacteria play a pivotal role in the lithification process by increasing the saturation index of calcium minerals within the mat. Strain L21-Syr-ABT was isolated from anoxic samples of a several centimeters-thick microbialite-forming cyanobacterial mat of a hypersaline lake on the Kiritimati Atoll (Kiribati, Central Pacific). The novel isolate was assigned to the family Desulfovibrionaceae within the Deltaproteobacteria. Available 16S rRNA-based population surveys obtained from discrete layers of the mat indicate that the occurrence of a species-level clade represented by strain L21-Syr-ABT is restricted to a specific layer of the suboxic zone, which is characterized by the presence of aragonitic spherulites. To elucidate a possible function of this sulfate-reducing bacterium in the mineral formation within the mat a comprehensive phenotypic characterization was combined with the results of a comparative genome analysis. Among the determined traits of strain L21-Syr-ABT, several features were identified that could play a role in the precipitation of calciummore » carbonate: (i) the potential deacetylation of polysaccharides and consumption of substrates such as lactate and sulfate could mobilize free calcium; (ii) under conditions that favor the utilization of formate and hydrogen, the alkalinity engine within the mat is stimulated, thereby increasing the availability of carbonate; (iii) the production of extracellular polysaccharides could provide nucleation sites for calcium mineralization. In addition, our data suggest the proposal of the novel species and genus Desulfohalovibrio reitneri represented by the type strain L21-Syr-ABT (=DSM 26903T = JCM 18662T).« less

Authors:
; ; ; ; ;
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1508654
Alternate Identifier(s):
OSTI ID: 1560580
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Published Article
Journal Name:
Frontiers in Microbiology
Additional Journal Information:
Journal Name: Frontiers in Microbiology Journal Volume: 10; Journal ID: ISSN 1664-302X
Publisher:
Frontiers Research Foundation
Country of Publication:
Switzerland
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; stromatolites; lithification; biofilm; alkalinity engine; sulfate reduction

Citation Formats

Spring, Stefan, Sorokin, Dimitry Y., Verbarg, Susanne, Rohde, Manfred, Woyke, Tanja, and Kyrpides, Nikos C. Sulfate-Reducing Bacteria That Produce Exopolymers Thrive in the Calcifying Zone of a Hypersaline Cyanobacterial Mat. Switzerland: N. p., 2019. Web. doi:10.3389/fmicb.2019.00862.
Spring, Stefan, Sorokin, Dimitry Y., Verbarg, Susanne, Rohde, Manfred, Woyke, Tanja, & Kyrpides, Nikos C. Sulfate-Reducing Bacteria That Produce Exopolymers Thrive in the Calcifying Zone of a Hypersaline Cyanobacterial Mat. Switzerland. doi:10.3389/fmicb.2019.00862.
Spring, Stefan, Sorokin, Dimitry Y., Verbarg, Susanne, Rohde, Manfred, Woyke, Tanja, and Kyrpides, Nikos C. Wed . "Sulfate-Reducing Bacteria That Produce Exopolymers Thrive in the Calcifying Zone of a Hypersaline Cyanobacterial Mat". Switzerland. doi:10.3389/fmicb.2019.00862.
@article{osti_1508654,
title = {Sulfate-Reducing Bacteria That Produce Exopolymers Thrive in the Calcifying Zone of a Hypersaline Cyanobacterial Mat},
author = {Spring, Stefan and Sorokin, Dimitry Y. and Verbarg, Susanne and Rohde, Manfred and Woyke, Tanja and Kyrpides, Nikos C.},
abstractNote = {Calcifying microbial mats in hypersaline environments are important model systems for the study of the earliest ecosystems on Earth that started to appear more than three billion years ago and have been preserved in the fossil record as laminated lithified structures known as stromatolites. It is believed that sulfate-reducing bacteria play a pivotal role in the lithification process by increasing the saturation index of calcium minerals within the mat. Strain L21-Syr-ABT was isolated from anoxic samples of a several centimeters-thick microbialite-forming cyanobacterial mat of a hypersaline lake on the Kiritimati Atoll (Kiribati, Central Pacific). The novel isolate was assigned to the family Desulfovibrionaceae within the Deltaproteobacteria. Available 16S rRNA-based population surveys obtained from discrete layers of the mat indicate that the occurrence of a species-level clade represented by strain L21-Syr-ABT is restricted to a specific layer of the suboxic zone, which is characterized by the presence of aragonitic spherulites. To elucidate a possible function of this sulfate-reducing bacterium in the mineral formation within the mat a comprehensive phenotypic characterization was combined with the results of a comparative genome analysis. Among the determined traits of strain L21-Syr-ABT, several features were identified that could play a role in the precipitation of calcium carbonate: (i) the potential deacetylation of polysaccharides and consumption of substrates such as lactate and sulfate could mobilize free calcium; (ii) under conditions that favor the utilization of formate and hydrogen, the alkalinity engine within the mat is stimulated, thereby increasing the availability of carbonate; (iii) the production of extracellular polysaccharides could provide nucleation sites for calcium mineralization. In addition, our data suggest the proposal of the novel species and genus Desulfohalovibrio reitneri represented by the type strain L21-Syr-ABT (=DSM 26903T = JCM 18662T).},
doi = {10.3389/fmicb.2019.00862},
journal = {Frontiers in Microbiology},
number = ,
volume = 10,
place = {Switzerland},
year = {2019},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.3389/fmicb.2019.00862

Citation Metrics:
Cited by: 1 work
Citation information provided by
Web of Science

Figures / Tables:

FIGURE 1 FIGURE 1: Phylogenetic tree inferred from 16S rRNA gene sequences showing the placement of strain L21-Syr-ABT within the Desulfovibrionaceae. The tree topology was reconstructed under the maximum-likelihood criterion and rooted using the 16S rRNA gene sequences of Desulfonatronum lacustre (AF418171), Desulfonatronospira thiodismutans (EU296537), Desulfonatronovibrio hydrogenovorans (X99234), Desulfovermiculus halophilus (DQ139408), Desulfohalobiummore » retbaense (CP001734), Desulfothermus naphthae (X80922), Desulfonauticus submarinus (FNIN01000014), Desulfoplanes formicivorans (LC017841), Desulfomicrobium baculatum (CP001629), and Desulfobacter postgatei (AGJR02000005) as outgroup (not shown). Accession numbers are given in parentheses. Support of a distinct branching by bootstrap analyses is indicated by symbols. Black dots at a distinct node indicate that bootstrap values of 95% or above (percentages of 1000 resamplings) were obtained with three different reconstruction methods, while gray dots indicate that values of 95% or above were obtained with two reconstruction methods. White dots indicate that bootstrap values of 75% or above were obtained with at least one reconstruction method. In such cases the values of 75% or above are given from left to right for the maximum-likelihood, neighbor-joining and maximum parsimony method. Letters and boxes shaded in different colors indicate distinct clades that were obtained also in trees based on the RpoB protein (Figure 2). Scale bar, 0.10 changes per nucleotide position.« less

Save / Share:

Works referenced in this record:

Microbialites: Organosedimentary Deposits of Benthic Microbial Communities
journal, January 1987

  • Burne, Robert V.; Moore, Linda S.
  • PALAIOS, Vol. 2, Issue 3
  • DOI: 10.2307/3514674

Sulfate reduction and thiosulfate transformations in a cyanobacterial mat during a diel oxygen cycle
journal, March 1994


Uncultivated microbes in need of their own taxonomy
journal, July 2017

  • Konstantinidis, Konstantinos T.; Rosselló-Móra, Ramon; Amann, Rudolf
  • The ISME Journal, Vol. 11, Issue 11
  • DOI: 10.1038/ismej.2017.113

Draft Genome Sequences for Three Mercury-Methylating, Sulfate-Reducing Bacteria
journal, June 2013

  • Brown, S. D.; Hurt, R. A.; Gilmour, C. C.
  • Genome Announcements, Vol. 1, Issue 4, Article No. e00618-13
  • DOI: 10.1128/genomeA.00618-13

STROMATOLITES IN PRECAMBRIAN CARBONATES: Evolutionary Mileposts or Environmental Dipsticks?
journal, May 1999


Desulfovibrio alkalitolerans sp. nov., a novel alkalitolerant, sulphate-reducing bacterium isolated from district heating water
journal, May 2006

  • Abildgaard, L.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 5
  • DOI: 10.1099/ijs.0.63909-0

rpoB gene as a novel molecular marker to infer phylogeny in Planctomycetales
journal, August 2013


Clostridium hathewayi sp. nov., from Human Faeces
journal, January 2001

  • Steer, Toni; Collins, Matthew D.; Gibson, Glenn R.
  • Systematic and Applied Microbiology, Vol. 24, Issue 3
  • DOI: 10.1078/0723-2020-00044

Rapid emergence of life shown by discovery of 3,700-million-year-old microbial structures
journal, August 2016

  • Nutman, Allen P.; Bennett, Vickie C.; Friend, Clark R. L.
  • Nature, Vol. 537, Issue 7621
  • DOI: 10.1038/nature19355

The standard operating procedure of the DOE-JGI Microbial Genome Annotation Pipeline (MGAP v.4)
journal, October 2015

  • Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/s40793-015-0077-y

Cellular Fatty Acid Composition of Desulfovibrio Species and Its Use in Classification of Sulfate-reducing Bacteria
journal, December 1992

  • Vainshtein, Mikhail; Hippe, Hans; Kroppenstedt, Reiner M.
  • Systematic and Applied Microbiology, Vol. 15, Issue 4
  • DOI: 10.1016/S0723-2020(11)80115-3

Desulfovibrio brasiliensis sp. nov., a moderate halophilic sulfate-reducing bacterium from Lagoa Vermelha (Brazil) mediating dolomite formation
journal, April 2005


Lipid composition of Halobacterium lacusprofundi
journal, January 1990


Metagenomic Analysis Suggests Modern Freshwater Microbialites Harbor a Distinct Core Microbial Community
journal, January 2016

  • White, Richard Allen; Chan, Amy M.; Gavelis, Gregory S.
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01531

dbCAN2: a meta server for automated carbohydrate-active enzyme annotation
journal, May 2018

  • Zhang, Han; Yohe, Tanner; Huang, Le
  • Nucleic Acids Research, Vol. 46, Issue W1
  • DOI: 10.1093/nar/gky418

LUD, a new protein domain associated with lactate utilization
journal, November 2013

  • Hwang, William C.; Bakolitsa, Constantina; Punta, Marco
  • BMC Bioinformatics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2105-14-341

Genome biology of a novel lineage of planctomycetes widespread in anoxic aquatic environments
journal, July 2018

  • Spring, Stefan; Bunk, Boyke; Spröer, Cathrin
  • Environmental Microbiology, Vol. 20, Issue 7
  • DOI: 10.1111/1462-2920.14253

The Photosynthetic Apparatus and Its Regulation in the Aerobic Gammaproteobacterium Congregibacter litoralis gen. nov., sp. nov
journal, March 2009


Genomic and phenotypic attributes of novel salinivibrios from stromatolites, sediment and water from a high altitude lake
journal, January 2014

  • Gorriti, Marta F.; Dias, Graciela M.; Chimetto, Luciane A.
  • BMC Genomics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2164-15-473

First genome sequences of Achromobacter phages reveal new members of the N4 family
journal, January 2014

  • Wittmann, Johannes; Dreiseikelmann, Brigitte; Rohde, Manfred
  • Virology Journal, Vol. 11, Issue 1
  • DOI: 10.1186/1743-422X-11-14

Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
journal, August 2014

  • Yarza, Pablo; Yilmaz, Pelin; Pruesse, Elmar
  • Nature Reviews Microbiology, Vol. 12, Issue 9
  • DOI: 10.1038/nrmicro3330

Microbially influenced formation of Mg-calcite and Ca-dolomite in the presence of exopolymeric substances produced by sulphate-reducing bacteria
journal, October 2013

  • Bontognali, Tomaso R. R.; McKenzie, Judith A.; Warthmann, Rolf J.
  • Terra Nova, Vol. 26, Issue 1
  • DOI: 10.1111/ter.12072

Genomic Encyclopedia of Type Strains, Phase I: The one thousand microbial genomes (KMG-I) project
journal, December 2013

  • Kyrpides, Nikos C.; Woyke, Tanja; Eisen, Jonathan A.
  • Standards in Genomic Sciences, Vol. 9, Issue 3
  • DOI: 10.4056/sigs.5068949

The Deep Subsurface Biosphere in Igneous Ocean Crust: Frontier Habitats for Microbiological Exploration
journal, January 2012

  • Edwards, Katrina J.; Fisher, Andrew T.; Wheat, C. Geoffrey
  • Frontiers in Microbiology, Vol. 3
  • DOI: 10.3389/fmicb.2012.00008

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation
journal, November 2010

  • Chan, Clara S.; Fakra, Sirine C.; Emerson, David
  • The ISME Journal, Vol. 5, Issue 4
  • DOI: 10.1038/ismej.2010.173

The rpoB gene as a tool for clinical microbiologists
journal, January 2009

  • Adékambi, Toïdi; Drancourt, Michel; Raoult, Didier
  • Trends in Microbiology, Vol. 17, Issue 1
  • DOI: 10.1016/j.tim.2008.09.008

Genomic Encyclopedia of Bacteria and Archaea: Sequencing a Myriad of Type Strains
journal, August 2014


Twenty years of the MEROPS database of proteolytic enzymes, their substrates and inhibitors
journal, November 2015

  • Rawlings, Neil D.; Barrett, Alan J.; Finn, Robert
  • Nucleic Acids Research, Vol. 44, Issue D1
  • DOI: 10.1093/nar/gkv1118

A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life
journal, August 2018

  • Parks, Donovan H.; Chuvochina, Maria; Waite, David W.
  • Nature Biotechnology, Vol. 36, Issue 10
  • DOI: 10.1038/nbt.4229

Formation of lithified micritic laminae in modern marine stromatolites (Bahamas); the role of sulfur cycling
journal, December 1998

  • Visscher, Pieter T.; Reid, R. Pamela; Bebout, Brad M.
  • American Mineralogist, Vol. 83, Issue 11-12 Part 2
  • DOI: 10.2138/am-1998-11-1236

OrthoANI: An improved algorithm and software for calculating average nucleotide identity
journal, February 2016

  • Lee, Imchang; Ouk Kim, Yeong; Park, Sang-Cheol
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 2
  • DOI: 10.1099/ijsem.0.000760

The Genetic Basis for Bacterial Mercury Methylation
journal, February 2013


Formation of stromatolite lamina at the interface of oxygenic-anoxygenic photosynthesis
journal, March 2018

  • Pace, A.; Bourillot, R.; Bouton, A.
  • Geobiology, Vol. 16, Issue 4
  • DOI: 10.1111/gbi.12281

TransportDB 2.0: a database for exploring membrane transporters in sequenced genomes from all domains of life
journal, November 2016

  • Elbourne, Liam D. H.; Tetu, Sasha G.; Hassan, Karl A.
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw1068

A Proposed Genus Boundary for the Prokaryotes Based on Genomic Insights
journal, April 2014

  • Qin, Q. -L.; Xie, B. -B.; Zhang, X. -Y.
  • Journal of Bacteriology, Vol. 196, Issue 12
  • DOI: 10.1128/JB.01688-14

Phylogenetic Analysis of a Microbialite-Forming Microbial Mat from a Hypersaline Lake of the Kiritimati Atoll, Central Pacific
journal, June 2013


Evidence for arsenic metabolism and cycling by microorganisms 2.7 billion years ago
journal, October 2014

  • Sforna, Marie Catherine; Philippot, Pascal; Somogyi, Andrea
  • Nature Geoscience, Vol. 7, Issue 11
  • DOI: 10.1038/ngeo2276

Desulfovibrio africanus subsp. uniflagellum subsp. nov., a sulfate-reducing bacterium from a uranium-contaminated subsurface aquifer
journal, August 2009

  • Castaneda-Carrion, I. N.; Sheik, C. S.; Krumholz, L. R.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 4
  • DOI: 10.1099/ijs.0.006668-0

High quality draft genome sequence and analysis of Pontibacter roseus type strain SRC-1T (DSM 17521T) isolated from muddy waters of a drainage system in Chandigarh, India
journal, January 2015

  • Mukherjee, Supratim; Lapidus, Alla; Shapiro, Nicole
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/1944-3277-10-8

Desulfotomaculum thermosubterraneum sp. nov., a thermophilic sulfate-reducer isolated from an underground mine located in a geothermally active area
journal, November 2006

  • Kaksonen, A. H.; Spring, S.; Schumann, P.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 56, Issue 11
  • DOI: 10.1099/ijs.0.64439-0

The SILVA ribosomal RNA gene database project: improved data processing and web-based tools
journal, November 2012

  • Quast, Christian; Pruesse, Elmar; Yilmaz, Pelin
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1219

Complete rpoB gene sequencing as a suitable supplement to DNA-DNA hybridization for bacterial species and genus delineation
journal, August 2008

  • Adekambi, T.; Shinnick, T. M.; Raoult, D.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 8
  • DOI: 10.1099/ijs.0.65440-0

Aerobic sulfate reduction in microbial mats
journal, March 1991


Processes of carbonate precipitation in modern microbial mats
journal, October 2009


ARB: a software environment for sequence data
journal, February 2004


Calcification of cyanobacterial mats in Solar Lake, Sinai
journal, January 1984


Commentary on the Hungate technique for culture of anaerobic bacteria
journal, December 1972


Microbes produce nanobacteria-like structures, avoiding cell entombment
journal, January 2008

  • Bontognali, Tomaso R. R.; Vasconcelos, Crisógono; Warthmann, Rolf J.
  • Geology, Vol. 36, Issue 8
  • DOI: 10.1130/G24755A.1

The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

A quick method for the determination of dissolved and precipitated sulfides in cultures of sulfate-reducing bacteria
journal, June 1985


Roles of HynAB and Ech, the Only Two Hydrogenases Found in the Model Sulfate Reducer Desulfovibrio gigas
journal, August 2013

  • Morais-Silva, F. O.; Santos, C. I.; Rodrigues, R.
  • Journal of Bacteriology, Vol. 195, Issue 20
  • DOI: 10.1128/JB.00411-13

Respiratory Quinones of Sulphate-Reducing and Sulphur-Reducing Bacteria: A Systematic Investigation
journal, July 1986


Sulfate Transporters in Dissimilatory Sulfate Reducing Microorganisms: A Comparative Genomics Analysis
journal, March 2018


Characterization of the first cultured representative of Verrucomicrobia subdivision 5 indicates the proposal of a novel phylum
journal, June 2016

  • Spring, Stefan; Bunk, Boyke; Spröer, Cathrin
  • The ISME Journal, Vol. 10, Issue 12
  • DOI: 10.1038/ismej.2016.84

Solar Lake (Sinai). 5. The sulfur cycle of the bcnthic cyanobacterial mats1: Solar Lake. 5.
journal, July 1977


The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes
preprint, March 2016


Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle
journal, February 2018

  • Anantharaman, Karthik; Hausmann, Bela; Jungbluth, Sean P.
  • The ISME Journal, Vol. 12, Issue 7
  • DOI: 10.1038/s41396-018-0078-0

High Diversity of Culturable Prokaryotes in a Lithifying Hypersaline Microbial Mat
journal, March 2015


IMG/M v.5.0: an integrated data management and comparative analysis system for microbial genomes and microbiomes
journal, October 2018

  • Chen, I-Min A.; Chu, Ken; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky901

A Diagnostic Reaction of Desulphovibrio desulphuricans
journal, February 1959


Microbially mediated carbonate precipitation in a hypersaline lake, Big Pond (Eleuthera, Bahamas): Microbially mediated carbonate precipitation
journal, August 2010


Active transport, substrate specificity, and methylation of Hg(II) in anaerobic bacteria
journal, May 2011

  • Schaefer, J. K.; Rocks, S. S.; Zheng, W.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 21
  • DOI: 10.1073/pnas.1105781108

Isolation of <i>Desulfovibrio intestinalis</i> sp. nov. from the hindgut of the lower termite <i>Mastotermes darwiniensis</i>
journal, January 1999

  • Fröhlich, Jürgen; Sass, Henrik; Babenzien, Hans-Dietrich
  • Canadian Journal of Microbiology, Vol. 45, Issue 2
  • DOI: 10.1139/cjm-45-2-145

Phylogenetic and environmental diversity of DsrAB-type dissimilatory (bi)sulfite reductases
journal, October 2014

  • Müller, Albert Leopold; Kjeldsen, Kasper Urup; Rattei, Thomas
  • The ISME Journal, Vol. 9, Issue 5
  • DOI: 10.1038/ismej.2014.208

Inside the alkalinity engine: the role of electron donors in the organomineralization potential of sulfate-reducing bacteria
journal, August 2012


Unravelling core microbial metabolisms in the hypersaline microbial mats of Shark Bay using high-throughput metagenomics
journal, May 2015

  • Ruvindy, Rendy; White III, Richard Allen; Neilan, Brett Anthony
  • The ISME Journal, Vol. 10, Issue 1
  • DOI: 10.1038/ismej.2015.87

    Works referencing / citing this record:

    List of new names and new combinations previously effectively, but not validly, published
    journal, July 2016

    • Oren, Aharon; Garrity, George M.
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 66, Issue 7
    • DOI: 10.1099/ijsem.0.001149

    List of new names and new combinations previously effectively, but not validly, published
    journal, April 2015

    • Oren, Aharon; Garrity, George M.
    • International Journal of Systematic and Evolutionary Microbiology, Vol. 65, Issue Pt_4
    • DOI: 10.1099/ijs.0.000178

      Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.