Expanding the genomic encyclopedia of Actinobacteria with 824 isolate reference genomes

Rekha Seshadri; Simon Roux; Katharina J Huber; Dongying Wu; Sora Yu; Dan Udwary; Lee Call; Stephen Nayfach; Richard L Hahnke; Rüdiger Pukall; James R White; Neha J Varghese; Cody Webb; Krishnaveni Palaniappan; Lorenz C Reimer; Joaquim Sardà; Jonathon Bertsch; Supratim Mukherjee; T B K Reddy; Patrick P Hajek; Marcel Huntemann; I-Min A Chen; Alex Spunde; Alicia Clum; Nicole Shapiro; Zong-Yen Wu; Zhiying Zhao; Yuguang Zhou; Lyudmila Evtushenko; Sofie Thijs; Vincent Stevens; Emiley A Eloe-Fadrosh; Nigel J Mouncey; Yasuo Yoshikuni; William B Whitman; Hans-Peter Klenk; Tanja Woyke; Markus Göker; Nikos C Kyrpides; Natalia N Ivanova

doi:10.1016/j.xgen.2022.100213

Expanding the genomic encyclopedia of Actinobacteria with 824 isolate reference genomes

Cell Genom. 2022 Nov 11;2(12):100213. doi: 10.1016/j.xgen.2022.100213. eCollection 2022 Dec 14.

Authors

Rekha Seshadri¹, Simon Roux¹, Katharina J Huber², Dongying Wu¹, Sora Yu³, Dan Udwary^{1

3}, Lee Call¹, Stephen Nayfach¹, Richard L Hahnke², Rüdiger Pukall², James R White⁴, Neha J Varghese¹, Cody Webb¹, Krishnaveni Palaniappan¹, Lorenz C Reimer², Joaquim Sardà², Jonathon Bertsch¹, Supratim Mukherjee¹, T B K Reddy¹, Patrick P Hajek¹, Marcel Huntemann¹, I-Min A Chen¹, Alex Spunde¹, Alicia Clum¹, Nicole Shapiro¹, Zong-Yen Wu³, Zhiying Zhao¹, Yuguang Zhou⁵, Lyudmila Evtushenko⁶, Sofie Thijs⁷, Vincent Stevens⁷, Emiley A Eloe-Fadrosh^{1

3}, Nigel J Mouncey^{1

3}, Yasuo Yoshikuni^{1

3

8

9

10}, William B Whitman¹¹, Hans-Peter Klenk¹², Tanja Woyke^{1

3}, Markus Göker², Nikos C Kyrpides^{1

3}, Natalia N Ivanova^{1

3}

Affiliations

¹ US Department of Energy Joint Genome Institute, Berkeley, CA, USA.
² Leibniz Institute DSMZ - German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.
³ Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.
⁴ Resphera Biosciences, Baltimore, MD, USA.
⁵ China General Microbiological Culture Collection Center, Beijing, China.
⁶ Pushchino Scientific Center for Biological Research of the Russian Academy of Sciences, All-Russian Collection of Microorganisms (VKM), Pushchino, Russia.
⁷ Center for Environmental Sciences, Environmental Biology, Hasselt University, Diepenbeek, Belgium.
⁸ Biological Systems and Engineering Division, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
⁹ Center for Advanced Bioenergy and Bioproducts Innovation, Lawrence Berkeley National Laboratory, Berkeley, CA 94720, USA.
¹⁰ Global Institution for Collaborative Research and Education, Hokkaido University, Hokkaido 060-8589, Japan.
¹¹ Department of Microbiology, University of Georgia, Athens, GA, USA.
¹² School of Biology, Newcastle University, Newcastle upon Tyne, UK.

Abstract

The phylum Actinobacteria includes important human pathogens like Mycobacterium tuberculosis and Corynebacterium diphtheriae and renowned producers of secondary metabolites of commercial interest, yet only a small part of its diversity is represented by sequenced genomes. Here, we present 824 actinobacterial isolate genomes in the context of a phylum-wide analysis of 6,700 genomes including public isolates and metagenome-assembled genomes (MAGs). We estimate that only 30%-50% of projected actinobacterial phylogenetic diversity possesses genomic representation via isolates and MAGs. A comparison of gene functions reveals novel determinants of host-microbe interaction as well as environment-specific adaptations such as potential antimicrobial peptides. We identify plasmids and prophages across isolates and uncover extensive prophage diversity structured mainly by host taxonomy. Analysis of >80,000 biosynthetic gene clusters reveals that horizontal gene transfer and gene loss shape secondary metabolite repertoire across taxa. Our observations illustrate the essential role of and need for high-quality isolate genome sequences.

Keywords: actinobacteria; comparative genomics; ecology; evolution; metagenomics; microbiology; mycobacteria; secondary metabolites.