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Title: Inference of Interactions in Cyanobacterial-Heterotrophic Co-Cultures via Transcriptome Sequencing

Abstract

We employed deep sequencing technology to identify transcriptional adaptation of the euryhaline unicellular cyanobacterium Synechococcus sp. PCC 7002 and the marine facultative aerobe Shewanella putrefaciens W3-18-1 to growth in a co-culture and infer the effect of carbon flux distributions on photoautotroph-heterotroph interactions. The overall transcriptome response of both organisms to co-cultivation was shaped by their respective physiologies and growth constraints. Carbon limitation resulted in the expansion of metabolic capacities which was manifested through the transcriptional upregulation of transport and catabolic pathways. While growth coupling occurred via lactate oxidation or secretion of photosynthetically fixed carbon, there was evidence of specific metabolic interactions between the two organisms. On one hand, the production and excretion of specific amino acids (methionine and alanine) by the cyanobacterium correlated with the putative downregulation of the corresponding biosynthetic machinery of Shewanella W3-18-1. On the other hand, the broad and consistent decrease of mRNA levels for many Fe-regulated Synechococcus 7002 genes during co-cultivation suggested increased Fe availability as well as more facile and energy-efficient mechanisms for Fe acquisition by the cyanobacterium. Furthermore, evidence pointed at potentially novel interactions between oxygenic photoautotrophs and heterotrophs related to the oxidative stress response as transcriptional patterns suggested that Synechococcus 7002 rather thanmore » Shewanella W3-18-1 provided scavenging functions for reactive oxygen species under co-culture conditions. This study provides an initial insight into the complexity of photoautotrophic-heterotrophic interactions and brings new perspectives of their role in the robustness and stability of the association.« less

Authors:
; ; ; ; ; ; ; ; ; ; ; ; ; ;
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1173028
Report Number(s):
PNNL-SA-98626
47445; KP1601010
DOE Contract Number:  
AC05-76RL01830
Resource Type:
Journal Article
Journal Name:
The ISME Journal, 8(11):2243-2255
Additional Journal Information:
Journal Name: The ISME Journal, 8(11):2243-2255
Country of Publication:
United States
Language:
English
Subject:
cyanobacterium; heterotroph/co-culture; interactions; transcriptome; next-generation sequencing; Environmental Molecular Sciences Laboratory

Citation Formats

Beliaev, Alex S., Romine, Margaret F., Serres, Margaret, Bernstein, Hans C., Linggi, Bryan E., Markillie, Lye Meng, Isern, Nancy G., Chrisler, William B., Kucek, Leo A., Hill, Eric A., Pinchuk, Grigoriy, Bryant, Donald A., Wiley, H. S., Fredrickson, Jim K., and Konopka, Allan. Inference of Interactions in Cyanobacterial-Heterotrophic Co-Cultures via Transcriptome Sequencing. United States: N. p., 2014. Web. doi:10.1038/ismej.2014.69.
Beliaev, Alex S., Romine, Margaret F., Serres, Margaret, Bernstein, Hans C., Linggi, Bryan E., Markillie, Lye Meng, Isern, Nancy G., Chrisler, William B., Kucek, Leo A., Hill, Eric A., Pinchuk, Grigoriy, Bryant, Donald A., Wiley, H. S., Fredrickson, Jim K., & Konopka, Allan. Inference of Interactions in Cyanobacterial-Heterotrophic Co-Cultures via Transcriptome Sequencing. United States. doi:10.1038/ismej.2014.69.
Beliaev, Alex S., Romine, Margaret F., Serres, Margaret, Bernstein, Hans C., Linggi, Bryan E., Markillie, Lye Meng, Isern, Nancy G., Chrisler, William B., Kucek, Leo A., Hill, Eric A., Pinchuk, Grigoriy, Bryant, Donald A., Wiley, H. S., Fredrickson, Jim K., and Konopka, Allan. Tue . "Inference of Interactions in Cyanobacterial-Heterotrophic Co-Cultures via Transcriptome Sequencing". United States. doi:10.1038/ismej.2014.69.
@article{osti_1173028,
title = {Inference of Interactions in Cyanobacterial-Heterotrophic Co-Cultures via Transcriptome Sequencing},
author = {Beliaev, Alex S. and Romine, Margaret F. and Serres, Margaret and Bernstein, Hans C. and Linggi, Bryan E. and Markillie, Lye Meng and Isern, Nancy G. and Chrisler, William B. and Kucek, Leo A. and Hill, Eric A. and Pinchuk, Grigoriy and Bryant, Donald A. and Wiley, H. S. and Fredrickson, Jim K. and Konopka, Allan},
abstractNote = {We employed deep sequencing technology to identify transcriptional adaptation of the euryhaline unicellular cyanobacterium Synechococcus sp. PCC 7002 and the marine facultative aerobe Shewanella putrefaciens W3-18-1 to growth in a co-culture and infer the effect of carbon flux distributions on photoautotroph-heterotroph interactions. The overall transcriptome response of both organisms to co-cultivation was shaped by their respective physiologies and growth constraints. Carbon limitation resulted in the expansion of metabolic capacities which was manifested through the transcriptional upregulation of transport and catabolic pathways. While growth coupling occurred via lactate oxidation or secretion of photosynthetically fixed carbon, there was evidence of specific metabolic interactions between the two organisms. On one hand, the production and excretion of specific amino acids (methionine and alanine) by the cyanobacterium correlated with the putative downregulation of the corresponding biosynthetic machinery of Shewanella W3-18-1. On the other hand, the broad and consistent decrease of mRNA levels for many Fe-regulated Synechococcus 7002 genes during co-cultivation suggested increased Fe availability as well as more facile and energy-efficient mechanisms for Fe acquisition by the cyanobacterium. Furthermore, evidence pointed at potentially novel interactions between oxygenic photoautotrophs and heterotrophs related to the oxidative stress response as transcriptional patterns suggested that Synechococcus 7002 rather than Shewanella W3-18-1 provided scavenging functions for reactive oxygen species under co-culture conditions. This study provides an initial insight into the complexity of photoautotrophic-heterotrophic interactions and brings new perspectives of their role in the robustness and stability of the association.},
doi = {10.1038/ismej.2014.69},
journal = {The ISME Journal, 8(11):2243-2255},
number = ,
volume = ,
place = {United States},
year = {2014},
month = {4}
}