Genomic insights into the physiology and ecology of the marine filamentous cyanobacterium Lyngbya majuscula

Abstract

Filamentous cyanobacteria of the genus Lyngbya are important contributors to coral reef ecosystems, occasionally forming dominant cover and impacting the health of many other co-occurring organisms. Moreover, they are extraordinarily rich sources of bioactive secondary metabolites, with 35% of all reported cyanobacterial natural products deriving from this single pantropical genus. However, the true natural product potential and life strategies of Lyngbya strains are poorly understood because of phylogenetic ambiguity, lack of genomic information, and their close associations with heterotrophic bacteria and other cyanobacteria. To gauge the natural product potential of Lyngbya and gain insights into potential microbial interactions, we sequenced the genome of Lyngbya majuscula 3L, a Caribbean strain that produces the tubulin polymerization inhibitor curacin A and the molluscicide barbamide, using a combination of Sanger and 454 sequencing approaches. Whereas ∼293,000 nucleotides of the draft genome are putatively dedicated to secondary metabolism, this is far too few to encode a large suite of Lyngbya metabolites, suggesting Lyngbya metabolites are strain specific and may be useful in species delineation. Our analysis revealed a complex gene regulatory network, including a large number of sigma factors and other regulatory proteins, indicating an enhanced ability for environmental adaptation or microbial associations. Although Lyngbya species are reported to fix nitrogen, nitrogenase genes were not found in the genome or by PCR of genomic DNA. Subsequent growth experiments confirmed that L. majuscula 3L is unable to fix atmospheric nitrogen. These unanticipated life history characteristics challenge current views of the genus Lyngbya. diazotrophy | polyketide synthase/nonribosomal peptide synthetase | mass spectrometry | harmful algal bloom | marine biology

Comparative genomics uncovers the prolific and distinctive metabolic potential of the cyanobacterial genus Moorea

“…All are annotated as photosynthetic (atmospheric carbon dioxide as primary carbon source), nondiazotrophic (absence of nitrogenase genes), capable of the biosynthesis of all proteinogenic amino acids (except for tyrosine and phenylalanine), and possessing the biosynthetic genes for important cofactors including CoA, cobalamin, biotin, flavin, NAD, heme, and thiamine. Additionally, the number of specialized sigma factors in the genomes of these four filamentous marine cyanobacteria strains, as previously discussed in Jones et al (21), are virtually the same (five specialized sigma factors per genome). Despite the significant similarity between the four genomes, some COG categories were indicative of a number of subtle genetic differences (see comparison of COG categories in Supporting Information).…”

Structure and activity of DmmA, a marine haloalkane dehalogenase

“…25 In addition, no CurN coding sequence was identified by amplification from M. producta (formerly L. majuscula) genomic DNA, nor was CurN located in the recently sequenced M. producta 3L genome. 26 Furthermore, the G þ C content of curN (61%) contrasts with the rest of the curacin biosynthetic gene cluster (45.5%). The scaffolds used to assemble the M. producta genome ranged from 37 to 66% G þ C content, with the great majority falling between 40 and 45%.…”

“…The scaffolds used to assemble the M. producta genome ranged from 37 to 66% G þ C content, with the great majority falling between 40 and 45%. 26 In addition, CurN (now referred to as DmmA (dehalogenase A from a marine microbe) in accord with other dehalogenases of unknown biological function 8 ) has high similarity ($50%) to HLDs from other marine bacteria, although none are from the cyanobacterial phyla. From these data, we conclude that curN (dmmA) is most likely a product of one of the organisms that grew in close association with the M. producta field isolate whose metagenomic DNA cosmid library was used to sequence the cur gene cluster.…”

Deep sequencing of non-ribosomal peptide synthetases and polyketide synthases from the microbiomes of Australian marine sponges

“…and C. concentrica (Fan et al, 2012), the TEFAP approach amplified reads that form a phylogenetic clade with C domains from the marine cyanobacteria Moorea producens (Jones et al, 2011) and Acaryochloris marina (Swingley et al, 2008). Within Scopalina sp.…”