Transovarial Transmission of Symbiotic Bacteria in &lt;I&gt;Mastotermes darwiniensis&lt;/I&gt; (Isoptera: Mastotermitidae): Ultrastructural Aspects and Phylogenetic Implications

Sacchi, Luciano; Nalepa, Christine A.; Lenz, Michael; Bandi, Claudio; Corona, S.; Grigolo, Aldo; Bigliardi, Elisa

doi:10.1603/0013-8746(2000)093[1308:ttosbi]2.0.co;2

Cited by 23 publications

(12 citation statements)

References 14 publications

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“…Tanning of the discrete outer covering is essentially complete prior to oothecal deposition (McKittrick 1964). M. darwiniensis is also homologous with cockroaches in the detailed mechanisms used to transfer bacterial fat body endosymbionts to the oocytes; these endosymbionts are absent in mantids (Sacchi et al 2000). We therefore agree with Ratcli¡e et al (1952), Watson & Gay (1991), Klass (1995) and Kristensen (1995) who suggested that the ootheca of M. darwiniensis is homologous with the oothecae of cockroaches.…”

Section: Discussionsupporting

confidence: 89%

The ootheca ofMastotermes darwiniensisFroggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae

Nalepa

Lenz²

2000

Proc. R. Soc. Lond. B

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The basal termite Mastotermes darwiniensis produces an egg mass, the nature of which is controversial. The debate centres on whether it is homologous with the oothecae of mantids and cockroaches and, if so, whether its simple structure is plesiomorphic or apomorphic within the Dictyoptera. To help resolve these issues we observed primary reproductives of M. darwiniensis during oviposition and examined the morphology of the reproductive product. Oviposition is cockroach-like in that the egg mass is assembled within the vestibulum and the eggs are issued externally in pairs. The reproductive product is an ootheca of the blattarian type. A distinct, tanned outer covering is stretched over the two parallel rows of eggs. No keel is present and no calcium oxalate crystals were apparent in the outer covering. We cannot rule out the possibility that the simple structure of the ootheca is plesiomorphic within Dictyoptera. However, based on (i) apomorphies shared by Mastotermes and Blattaria, and (ii) the life habits of Isoptera, a secondary reduction is the more plausible explanation.

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Section: Discussionsupporting

confidence: 89%

The ootheca ofMastotermes darwiniensisFroggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae

Nalepa

Lenz²

2000

Proc. R. Soc. Lond. B

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“…These effects were attributed to the elimination of Blattabacterium, which mobilizes nitrogen from urate waste deposits within the fat tissue. It also provides vitamins, proteins, and essential amino acids to the roach (3,4,54,59). Although Z. angusticollis lacks an association with Blattabacterium (59), other bacteria, including the rifampin-eliminated Bacteroidetes and Treponema, are similarly involved in nitrogen fixation (11,13,35,43,46) and/or the production of NH 3 from uric acid (52,59,66).…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

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

Rosengaus

Zecher

Schultheis

et al. 2011

Appl Environ Microbiol

108

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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...

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“…The wood-feeding, "lower" termite Mastotermes darwiniensis is an exception among termites in that it, like cockroaches, maintains Blattabacterium within its fat bodies and transmits the endosymbiont transovarially to its offspring (38,68). Mastotermes is a deeply branching termite lineage (6,30), and it shares other morphological and reproductive similarities with cockroaches (14,19,55).…”

mentioning

confidence: 99%

Genome Shrinkage and Loss of Nutrient-Providing Potential in the Obligate Symbiont of the Primitive Termite Mastotermes darwiniensis

Sabree

Huang

Arakawa

et al. 2012

Appl Environ Microbiol

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Beneficial microbial associations with insects are common and are classified as either one or a few intracellular species that are vertically transmitted and reside intracellularly within specialized organs or as microbial assemblages in the gut. Cockroaches and termites maintain at least one if not both beneficial associations. Blattabacterium is a flavobacterial endosymbiont of nearly all cockroaches and the termite Mastotermes darwiniensis and can use nitrogenous wastes in essential amino acid and vitamin biosynthesis. Key changes during the evolutionary divergence of termites from cockroaches are loss of Blattabacterium, diet shift to wood, acquisition of a specialized hindgut microbiota, and establishment of advanced social behavior. Termite gut microbes collaborate to fix nitrogen, degrade lignocellulose, and produce nutrients, and the absence of Blattabacterium in nearly all termites suggests that its nutrient-provisioning role has been replaced by gut microbes. M. darwiniensis is a basal, extant termite that solely retains Blattabacterium, which would show evidence of relaxed selection if it is being supplanted by the gut microbiome. This termite-associated Blattabacterium genome is ϳ8% smaller than cockroach-associated Blattabacterium genomes and lacks genes underlying vitamin and essential amino acid biosynthesis. Furthermore, the M. darwiniensis gut microbiome membership is more consistent between individuals and includes specialized termite gut-associated bacteria, unlike the more variable membership of cockroach gut microbiomes. The M. darwiniensis Blattabacterium genome may reflect relaxed selection for some of its encoded functions, and the loss of this endosymbiont in all remaining termite genera may result from its replacement by a functionally complementary gut microbiota.

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Transovarial Transmission of Symbiotic Bacteria in <I>Mastotermes darwiniensis</I> (Isoptera: Mastotermitidae): Ultrastructural Aspects and Phylogenetic Implications

Cited by 23 publications

References 14 publications

The ootheca ofMastotermes darwiniensisFroggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae

The ootheca ofMastotermes darwiniensisFroggatt (Isoptera: Mastotermitidae): homology with cockroach oothecae

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

Genome Shrinkage and Loss of Nutrient-Providing Potential in the Obligate Symbiont of the Primitive Termite Mastotermes darwiniensis

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