Marine-derived myxobacteria of the suborder Nannocystineae: An underexplored source of structurally intriguing and biologically active metabolites

Abstract

Myxobacteria are famous for their ability to produce most intriguing secondary metabolites. Till recently, only terrestrial myxobacteria were in the focus of research. In this review, however, we discuss marine-derived myxobacteria, which are particularly interesting due to their relatively recent discovery and due to the fact that their very existence was called into question. The to-date-explored members of these halophilic or halotolerant myxobacteria are all grouped into the suborder Nannocystineae. Few of them were chemically investigated revealing around 11 structural types belonging to the polyketide, non-ribosomal peptide, hybrids thereof or terpenoid class of secondary metabolites. A most unusual structural type is represented by salimabromide from Enhygromyxa salina. In silico analyses were carried out on the available genome sequences of four bacterial members of the Nannocystineae, revealing the biosynthetic potential of these bacteria.

Keywords: Enhygromyxa; Nannocystineae; genome mining; myxobacteria; natural products.

Figure 1

Structures of cystobactamids 507, 919-1 and 919-2.

Figure 2

Structures of aurafuron A and corallopyronin A.

Figure 3

Structures of ixabepilone and capecitabine.

Figure 4

Structures of DKxanthene-534 and myxochelin A.

Figure 5

Phylogenetic tree of halotolerant and halophilic myxobacteria. The neighbor-joining tree is based on a multiple sequence alignment (MSA) of the 16S rDNA sequences. The terrestrial myxobacteria Myxococcus xanthus DK1622 and Sorangium cellulosum Soce56 as well as Escherichia albertii DM104 are included for comparison (see Supporting Information File 1 for the sequences used; the MSA was computed using Clustal Omega).

Figure 6

Structure of nannocystin A.

Figure 7

Structure of phenylnannolones A–C.

Figure 8

Structures of the pyrronazols, dihydroxyphenazin and 1-hydroxyphenazin-6-yl-α-D-arabinofuranoside.

Figure 9

Structures of nannozinones A + B and nannochelin A from N. pusilla strain MNa10913.

Figure 10

Structure of haliangicin from H. ochraceum.

Figure 11

Structure of haliamide from H. ochraceum SMP-2.

Figure 12

Structures of salimabromide, enhygrolides A + B and salimyxins A + B.

Figure 13

Structures of miuraenamides A–F from P. miuraensis.