The Ultramicrobacterium “
            <i>Elusimicrobium minutum</i>
            ” gen. nov., sp. nov., the First Cultivated Representative of the Termite Group 1 Phylum

111

The disruption of host-symbiont interactions through the use of antibiotics can help elucidate microbial functions that go beyond short-term nutritional value. Termite gut symbionts have been studied extensively, but little is known about their impact on the termite's reproductive output. Here we describe the effect that the antibiotic rifampin has not only on the gut microbial diversity but also on the longevity, fecundity, and weight of two termite species, Zootermopsis angusticollis and Reticulitermes flavipes. We report three key findings: (i) the antibiotic rifampin, when fed to primary reproductives during the incipient stages of colony foundation, causes a permanent reduction in the diversity of gut bacteria and a transitory effect on the density of the protozoan community; (ii) rifampin treatment reduces oviposition rates of queens, translating into delayed colony growth and ultimately reduced colony fitness; and (iii) the initial dosages of rifampin had severe long-term fitness effects on Z. angusticollis. Taken together, our findings demonstrate that the antibiotic-induced perturbation of the microbial community is associated with prolonged reductions in longevity and fecundity. A causal relationship between these changes in the gut microbial population structures and fitness is suggested by the acquisition of opportunistic pathogens and incompetence of the termites to restore a pretreatment, native microbiota. Our results indicate that antibiotic treatment significantly alters the termite's microbiota, reproduction, colony establishment, and ultimately colony growth and development. We discuss the implications for antimicrobials as a new application to the control of termite pest species.The long-standing associations between termites and prokaryotic and eukaryotic microorganisms have been crucial to the evolutionary and ecological success of this social insect group. The presence of cellulolytic microorganisms in the hindguts of termites is one of the key events that allowed termites to thrive on nitrogenously deficient food resources (49, 63). Fossil records (80) and the similarity in gut flora and other microbial endosymbionts with those of their roach relatives (59) support the hypothesis that these associations existed in the termite ancestor (3,50,59). Termite gut symbionts reside in the lumen or are attached to the wall of the hindgut region and can represent more than 40% of the termite's weight (6). They are horizontally transmitted through coprophagy, a common behavior in termites. Indeed, the need for transfaunation of hindgut symbionts has been proposed as one of the main factors favoring group living (44) and specifically favoring the evolution and maintenance of termite sociality (18). However, little is known about the impact that termite gut symbionts have beyond their role in cellulose degradation and host nutrition.Here we report on the impact that antibiotic treatment has on the reproductive survival and fecundity of the dampwood termite Zootermopsis angusticollis and the Eastern su...

Section: Discussionmentioning

confidence: 99%

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confidence: 99%

Disruption of the Termite Gut Microbiota and Its Prolonged Consequences for Fitness

Rosengaus

Zecher

Schultheis

et al. 2011

111

“…Meanwhile, numerous sequences affiliated with this phylum have also been retrieved from habitats other than termite guts. They form several deep-branching lineages comprising sequences derived not only from intestinal tracts but also from soils, sediments, and contaminated aquifers (14,20).Recently, we were able to isolate strain Pei191 T , the first pure-culture representative of the TG1 phylum, from the gut of a humivorous scarab beetle larva, Pachnoda ephippiata (14). Based on the 16S rRNA gene sequence, strain Pei191…”

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confidence: 99%

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confidence: 99%

Genomic Analysis of “ Elusimicrobium minutum ,” the First Cultivated Representative of the Phylum “ Elusimicrobia ” (Formerly Termite Group 1)

Herlemann

Geissinger

Ikeda-Ohtsubo

et al. 2009

Organisms of the candidate phylum termite group 1 (TG1) are regularly encountered in termite hindguts but are present also in many other habitats. Here, we report the complete genome sequence (1.64 Mbp) of "Elusimicrobium minutum" strain Pei191 T , the first cultured representative of the TG1 phylum. We reconstructed the metabolism of this strictly anaerobic bacterium isolated from a beetle larva gut, and we discuss the findings in light of physiological data. E. minutum has all genes required for uptake and fermentation of sugars via the Embden-Meyerhof pathway, including several hydrogenases, and an unusual peptide degradation pathway comprising transamination reactions and leading to the formation of alanine, which is excreted in substantial amounts. The presence of genes encoding lipopolysaccharide biosynthesis and the presence of a pathway for peptidoglycan formation are consistent with ultrastructural evidence of a gram-negative cell envelope. Even though electron micrographs showed no cell appendages, the genome encodes many genes putatively involved in pilus assembly. We assigned some to a type II secretion system, but the function of 60 pilE-like genes remains unknown. Numerous genes with hypothetical functions, e.g., polyketide synthesis, nonribosomal peptide synthesis, antibiotic transport, and oxygen stress protection, indicate the presence of hitherto undiscovered physiological traits. Comparative analysis of 22 concatenated single-copy marker genes corroborated the status of "Elusimicrobia" (formerly TG1) as a separate phylum in the bacterial domain, which was so far based only on 16S rRNA sequence analysis.At least half of the phylum-level lineages within the domain Bacteria do not comprise pure cultures but are, rather, represented only by 16S rRNA gene sequences of environmental origin (43). The number of such candidate phyla is still growing, and the biology of the members of these phyla is usually completely obscure. The first sequences of the candidate phylum termite group 1 (TG1) (23) were obtained from the hindgut of the termite Reticulitermes speratus, where they represent a substantial portion of the gut microbiota (21, 41). Meanwhile, numerous sequences affiliated with this phylum have also been retrieved from habitats other than termite guts. They form several deep-branching lineages comprising sequences derived not only from intestinal tracts but also from soils, sediments, and contaminated aquifers (14,20).Recently, we were able to isolate strain Pei191 T , the first pure-culture representative of the TG1 phylum, from the gut of a humivorous scarab beetle larva, Pachnoda ephippiata (14). Based on the 16S rRNA gene sequence, strain Pei191T is a member of the "intestinal cluster," which consists of sequences derived from invertebrate guts and cow rumen (20) and is only distantly related to the so-called "endomicrobia," a lineage of TG1 bacteria comprising endosymbionts of termite gut protozoa (24,42,54). It is an obligately anaerobic ultramicrobacterium that grows heterotrophically on g...

“…The origin of these lineages remains unclear, but their detection also in the guts of several cockroaches (15)(16)(17), the closest relatives of termites, together with occasional evidence of cocladogenesis with the termite hosts (18,19) has given rise to the hypothesis that the bacterial microbiota of extant termites and cockroaches is derived from their common dictyopteran ancestors.…”

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confidence: 99%

The Cockroach Origin of the Termite Gut Microbiota: Patterns in Bacterial Community Structure Reflect Major Evolutionary Events

Dietrich

Köhler

Brune

2014

Self Cite

221

339

Termites digest wood and other lignocellulosic substrates with the help of their intestinal microbiota. While the functions of the symbionts in the digestive process are slowly emerging, the origin of the bacteria colonizing the hindgut bioreactor is entirely unknown. Recently, our group discovered numerous representatives of bacterial lineages specific to termite guts in a closely related omnivorous cockroach, but it remains unclear whether they derive from the microbiota of a common ancestor or were independently selected by the gut environment. Here, we studied the bacterial gut microbiota in 34 species of termites and cockroaches using pyrotag analysis of the 16S rRNA genes. Although the community structures differed greatly between the major host groups, with dramatic changes in the relative abundances of particular bacterial taxa, we found that the majority of sequence reads belonged to bacterial lineages that were shared among most host species. When mapped onto the host tree, the changes in community structure coincided with major events in termite evolution, such as acquisition and loss of cellulolytic protists and the ensuing dietary diversification. UniFrac analysis of the core microbiota of termites and cockroaches and construction of phylogenetic tree of individual genus level lineages revealed a general host signal, whereas the branching order often did not match the detailed phylogeny of the host. It remains unclear whether the lineages in question have been associated with the ancestral cockroach since the early Cretaceous (cospeciation) or are diet-specific lineages that were independently acquired from the environment (host selection).