Genomes of Novel Myxococcota Reveal Severely Curtailed Machineries for Predation and Cellular Differentiation

Abstract

Cultured Myxococcota are predominantly aerobic soil inhabitants, characterized by their highly coordinated predation and cellular differentiation capacities. Little is currently known regarding yet-uncultured Myxococcota from anaerobic, non-soil habitats. We analyzed genomes representing one novel order (o__JAFGXQ01) and one novel family (f__JAFGIB01) in the Myxococcota from an anoxic freshwater spring (Zodletone spring) in Oklahoma, USA. Compared to their soil counterparts, anaerobic Myxococcota possess smaller genomes, and a smaller number of genes encoding biosynthetic gene clusters (BGCs), peptidases, one- and two-component signal transduction systems, and transcriptional regulators. Detailed analysis of thirteen distinct pathways/processes crucial to predation and cellular differentiation revealed severely curtailed machineries, with the notable absence of homologs for key transcription factors (e.g. FruA and MrpC), outer membrane exchange receptor (TraA), and the majority of sporulation-specific and A-motility-specific genes. Further, machine-learning approaches based on a set of 634 genes informative of social lifestyle predicted a non-social behavior for Zodletone Myxococcota. Metabolically, Zodletone Myxococcota genomes lacked aerobic respiratory capacities, but encoded genes suggestive of fermentation, dissimilatory nitrite reduction, and dissimilatory sulfate-reduction (in f_JAFGIB01) for energy acquisition. We propose that predation and cellular differentiation represent a niche adaptation strategy that evolved circa 500 Mya in response to the rise of soil as a distinct habitat on earth. Importance The Myxococcota is a phylogenetically coherent bacterial lineage that exhibits unique social traits. Cultured Myxococcota are predominantly aerobic soil-dwelling microorganisms that are capable of predation and fruiting body formation. However, multiple yet-uncultured lineages within the Myxococcota have been encountered in a wide range of non-soil, predominantly anaerobic habitats; and the metabolic capabilities, physiological preferences, and capacity of social behavior of such lineages remain unclear. Here, we analyzed genomes recovered from a metagenomic analysis of an anoxic freshwater spring in Oklahoma, USA that represent novel, yet-uncultured, orders and families in the Myxococcota. The genomes appear to lack the characteristic hallmarks for social behavior encountered in Myxococcota genomes, and displayed a significantly smaller genome size and a smaller number of genes encoding biosynthetic gene clusters, peptidases, signal transduction systems, and transcriptional regulators. Such perceived lack of social capacity was confirmed through detailed comparative genomic analysis of thirteen pathways associated with Myxococcota social behavior, as well as the implementation of machine learning approaches to predict social behavior based on genome composition. Metabolically, these novel Myxococcota are predicted to be strict anaerobes, utilizing fermentation, nitrate reduction, and dissimilarity sulfate reduction for energy acquisition. Our results highlight the broad patterns of metabolic diversity within the yet-uncultured Myxococcota and suggest that the evolution of predation and fruiting body formation in the Myxococcota has occurred in response to soil formation as a distinct habitat on earth.

HT-SIP: A semi-automated Stable Isotope Probing pipeline identifies interactions in the hyphosphere of arbuscular mycorrhizal fungi

“…Previous GWAS analysis indicates that Myxococcota have many prey-specific genes, rather than a general set of antimicrobial genes, which likely enable them to target a broad prey range [74]. Our analysis of the Fen-1088 MAGs also points to a large arsenal of proteases that may be used to consume prey, these are also found in many Myxococcota type species [65]. However, the relative lack of GH18 chitinase genes suggests this family may not be chitinolytic or may have low chitin degradation efficiency, as highly efficient chitinolytic organisms are thought to produce multiple types of chitinases [75, 76].…”

“…10 APE- 13 C more enriched than the AMF and ranged from 30-32% APE- 13 C ( Figure 3c , mCT241). Compared to a set of Mycococcota type species genomes [65], these three Fen-1088 MAGs contain similar amounts of genes associated with predation, such as potential cell lysis CAZyme families (7 GH13 genes, 5-7 GH23 genes) and protease genes (203-225 MEROPS protease homologs) (Supplemental Table S5). Two of the MAGs contain a chitinase gene (mCT114, mCT215) (Supplemental Table S6).…”

“…Two of the MAGs contain a chitinase gene (mCT114, mCT215) (Supplemental Table S6). However, these highly enriched MAGs were enriched in glycoside hydrolases and polysaccharide lyases that are atypical for Myxococcota type species [65], such as GH29 (α-fucosidases), GH109 (α-N-acetylgalactosaminidases), GH8 (β-1,4 linkages, such as those found in plant cell walls), PL6 (alginate and non-alginate lyases [66]), and PL14 (lyases of unknown function, including poly(b-mannuronate) lyase). These genomic differences are also apparent across the Myxococcota MAGs from this study, where the highly 13 C-enriched Fen-1088 MAGs consistently contained more PL6 and GH29 homologs than less-enriched Myxococcota ( Figure 5 ).…”

“…Eight Myxococcota MAGs ranged in APE- 13 C from 12-32%, and seven of these were from the littleknown Polyangia family Fen-1088 that is known only from metagenomic sequencing (only 31 MAGs in the Genome Taxonomy Database (GTDB)) (accessed June 2022) [64]. Similar to many Myxococcota [65], Fen-1088 have high GC contents (68-71%) and large genome sizes (3.5-7.8 Mbp) (Supplemental Table S3). Three highly-enriched Fen-1088 MAGs (mCT241, mCT215, mCT114) were ca.…”

Supplementation of Dietary Crude Lentinan Improves the Intestinal Microbiota and Immune Barrier in Rainbow Trout (Oncorhynchus mykiss) Infected by Infectious Hematopoietic Necrosis Virus

“…Similar to the spring viremia of carp virus ( 57 ), IHNV significantly increased the intestinal microbial α diversity in rainbow trout ( P <0.05). Mycobacteria (Actinobacteria) and Nannocystis (Myxococcota) are prevalent in soil and aquatic environments and are well known for causing disease in animals and humans ( 58 , 59 ). They might cause local hypoxia and further result in the tissue oxidative injury ( 60 ).…”